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The neurological evaluation scale (NES): A structured instrument for the assessment of neurological signs in schizophrenia
335
Psyc.hiatr_yResearch. 21,335-350 Elsevier
The Neurological Evaluation Scale (NES): A Structured Instrument for the Assessment of Neurological Signs in Schizophrenia Robert W. Buchanan
and Douglas
W. Heinrichs
Received January 22, 1988; revised version received August 17, 1988; accepted September 1988.
19.
Abstract. The significance of neurological signs in schizophrenia is poorly understood. In part, this may reflect the marked variability in the methods of ascertainment in previous studies. The Neurological Evaluation Scale (NES) is designed to standardize the assessment of neurological impairment in schizophrenia. The battery consists of 26 items. Data on the interrater reliability for total score, functional areas of interest, and individual items are presented. Preliminary validity data demonstrate the abiIity of the battery to discriminate patients with schizophrenia from nonpsychiatric controls. Key Words. Neurological
signs, assessment,
schizophrenia.
During the last two decades there has been a growing appreciation of the biological underpinnings of most major psychiatric syndromes including schizophrenia. This coincides with a major reawakening of interest in clinical problems at the interface of psychiatry and neurology, as reflected in the terms “neuropsychiatry” and “behavioral neurology” (Pincus and Tucker, 1974; Cummings, 1985; Mesulam, 1985; Hales and Yudofsky, 1987). In part, this is a response to the profound impact of psychotropic medication on the course of these disorders, but the availability of ever more sophisticated techniques for the biochemical, anatomical, and physiological examination of the brain has been a pivotal factor. In particular, advances in brain imaging have stimulated efforts to characterize the neuropathology of schizophrenia, and the “neurology of schizophrenia” has drawn increased research interest (Henn and Nasrallah, 1982; Andreasen, 1986; Nasrallah and Weinberger, 1986). Imaging studies have largely concentrated on image quantification, but there is a need for precise behavioral and clinical assessments to interpret these findings (Roland et al., 1987), including careful attention to the clinical manifestations of the neurological processes that accompany schizophrenic disorders. There is a long history, in schizophrenia, of anecdotal reports and descriptions of abnormalities on clinical neurological examination. In the past 25 years, a number of systematic surveys and controlled studies of neurological abnormalities have appeared in the literature. In reviewing this literature (Heinrichs and Buchanan, 1988), we found 19 studies that allowed comparisons between patients with schizophrenia
Robert W. Buchanan, M.D., and Douglas W. Heinrichs, M.D., are Assistant Professors of Psychiatry, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD. (Reprint requests to Dr. R.W. Buchanan, USA.) 0165-I 78 I /89/%03.50
Maryland
Psychiatric
@ 1989 Elsevier Scientific
Research
Publishers
Center,
Ireland
P.O. Box 21247, Baltimore,
Ltd.
MD 21228,
336 and controls. Without exception, there was an increased prevalence of neurological signs in schizophrenic patients compared to nonpsychiatric controls, and in most studies more neurological abnormalities were present in schizophrenic patients than in mixed diagnostic and affective disorder groups. Furthermore, evidence suggests that neurological abnormalities may relate to symptom dimensions, course of illness, and family history of schizophrenia, as well as being present in individuals at high risk before the onset of their illness (Heinrichs and Buchanan, 1988). Yet, for all this, abnormal neurological signs have received relatively little attention from investigators or clinicians. This neglect may stem, in part, from the belief that these findings are ambiguous, unreal, fleeting, nonreproducible, nonlocalizing, and uninterpretable-a viewpoint reflected in the frequent designation of these findings as “neurological soft signs.” However, our failure to understand the meaning of neurological symptoms in schizophrenia is probably more reflective of a limitation in our knowledge than a “softness” in the findings themselves. If neurological signs are to be an object of serious investigation, then precise and reproducible methods of assessment are needed. There is tremendous variability among existing studies in how signs are elicited and rated, and for many reports the exact methods are not described (Heinrichs and Buchanan, 1988). Many studies simply refer to a “comprehensive neurological examination.” Those studies that do specify methods tend to be the ones that focus on a specific and limited area of neurological abnormality. Less than half of the existing studies even mention reliability, though reliability coefficients, when evaluated, are usually quite acceptable. However, only one study has described a detailed and rigorous reliability exercise (Quitkin et al., 1976). Other important questions, such as temporal stability, practice effect, effect of medication, and impact of current clinical state, have not been adequately addressed. In this report, we present a structured neurological examination that addresses the areas of neurological impairment that have been consistently found in schizophrenia, a demonstration of the reliability of the examination, and preliminary data on its validity.
Construction of the Instrument A thorough search of the English-language literature focused on systematic surveys and controlled studies of clinical neurological evaluations of adult and adolescent patients with schizophrenia (Heinrichs and Buchanan, 1988). Specific signs representing areas of frequent impairment noted across multiple studies were selected. Dysfunction in three functional areas of interest (based on conceptual considerations of neuroanatomy and function) emerged from the review: 1. Integrative sensory dysfunction, reflected in items such as bilateral extinction, agraphesthesia, astereognosis, right/ left confusion, and impaired audiovisual integration. 2. Motor incoordination, reflected in items such as tandem walk, finger to nose, finger to thumb opposition, and dysdiadochokinesis. 3. Impaired sequencing of complex motor acts, reflected in items such as those used by Luria (1966), including the fist-ring, fist-edge-palm, and Ozeretski tests. In addition, abnormalities in eye movements (Stevens, 1982), frontal release signs (COX and Ludwig, 1979), and short-term memory (Broga and Neufield, 1981) have been frequently
337 observed. In contrast, primary sensory modalities, motor strength, and reflexes were characteristically intact in the schizophrenia cohorts previously studied (Heinrichs and Buchanan, 1988). From these considerations a battery of 26 discrete items, of which 14 items are tested and scored separately for the right and left sides of the body, was assembled. The instrument includes representative items from the three functional areas of interest, plus the assessment of cerebral dominance, short-term memory, frontal release signs, and eye movement abnormalities. All items are judged to be easily administered by a clinician at the bedside or in a consulting room with minimal equipment needed. A fixed order of administration is devised relating to ease of administration rather than conceptual categories. The procedure for administering each item is specified and standardized. Each item is scored on a 3-point scale: 0 = no abnormality; 1q mild, but definite impairment; and 2 = marked impairment, except for the snout and suck reflexes which are scored either as a 0 or 2. Descriptive anchors are provided for each score to facilitate standardized judgments (see Appendix). In addition to item scores and total score (sum of all items), subsets of items are totaled to yield scores for the three functional areas of interest discussed above: sensory integration, motor coordination, and sequencing of complex motor acts. The validity of these categories awaits further empirical assessment, and other categories may emerge from future analytic or conceptual approaches.
Reliability assess the interrater reliability using the battery, the authors simultaneously examined 46 subjects. Thirty-nine of the subjects were patients with a diagnosis of either DSM-III schizophrenia or schizophreniform disorder (American Psychiatric Association, 1980) or Research Diagnostic Criteria (RDC) schizoaffective, mainly schizophrenic disorder (Spitzer et al., 1978), and seven were normal controls. The raters scored the battery independently, alternating which rater conducted the examination. The interclass correlations for total score were 0.95; for sensory integration (SI), 0.99; for motor coordination (MC), 0.71; and for sequencing of complex motor acts (SQ), 0.89. Interclass correlations for each item are shown on Table 1. The interclass correlations were 2 0.90 for 14 items, 0.80-0.89 for 9 items, 0.70-0.79 for 7 items, 0.60-0.69 for 5 items, 0.50 to 0.59 for 3 items, and <0.50 for 3 items. The last three were rarer items, each occurring in < 10% of subjects. To determine the ability to train others to use the instrument reliably, one of the authors (R.W.B.) trained a nurse and a nonclinician research assistant and then conducted a reliability study with each. The reliability studies were conducted in the same manner as described for the two authors. Training, including the reliability exercise, took approximately 20 hours in each case. For the nurse, the interclass correlations for total score, SI, MC, and SQ, based on the examination of 15 subjects, were 0.88, 0.97, 0.72, and 0.80. The respective interclass correlations for the research assistant, based on the examination of 14 subjects, were 0.90, 0.98, 0.75, and 0.80.
To
Validity As a first step in the assessment of the validity of the instrument, we examined its ability to differentiate between schizophrenic outpatients and nonpatient controls. All of the subjects were examined by one of the authors. The patient group comprised 98 patients with either DSM-III schizophrenia or schizophreniform disorder or RDC schizoaffective disorder, mainly schizophrenic. The mean duration of illness was 8.4 years. The mean age was 32.1 years (SD = 8.3 years); 71% were male; 47% were black;
338 Table 1. Neurological Evaluation Scale: Interclass correlations for each item % with positive sign Item
Controls
Schizophrenics
(n = 50)
(n = 98)
F
P
72.4 7.1 14.3 42.8 46.9 19.4 74.5
28.00 2.75 5.49 0.02 1.92 -
0.00001 0.01 0.02 0.89 0.168 -
0.50
0.482
1.00 1.00 0.95 1.00 1.00 1.00 0.93
18.4
9.35
0.003
0.87
4.1
0.07
0.795
1 .oo
13.2
2.00
0.160
0.57
8.2
0.14
0.681
0.77
18.4 49.0 44.9
4.66 9.39 16.42
0.032 0.0003 0.0001
0.77 0.80 0.72
31.6 28.6 41.8 29.6 37.8 31.6
7.75 11.94 6.66 9.03 2.93 2.53
0.006 0.0007 0.011 0.003 0.089 0.114
0.73 0.67 0.69 0.88 0.95 0.83
27.6
11..09
0.001
0.85
30.6 7.1 24.5 29.6 59.2 61.2 85.7 38.8 41.8 43.9 43.9 18.4 20.4 12.2 15.3 49.0 1.0 7.1 8.2 13.3
14.51 -
0.0002 -
3.55 4.29 32.77 25.06 34.58 1.53 2.49 2.18 1.75 1.95 7.60 8.68 8.17 0.78 -
0.062 0.04 0.00001 0.00001 0.00001 0.218 0.017 0.142 0.188 0.165 0.007 0.004 0.005 0.378 -
0.81 0.88 0.58 0.64 0.94 0.99 0.97 0.56 0.75 0.90 0.72 0.67 0.77 0.86 0.95 0.81 0.0 0.44 0.14 0.60
Sensory Integration 28.0 A-V integration 2.0 Stereognosis, R 4.0 Stereognosis, L 46.0 Graphesthesia, R 38.0 Graphesthesia, L 0.0 Extinction 64.0 R/L confusion Motor Coordination 4.0 Tandem walk Rapid alternating 4.0 movements, R Rapid alternating 4.0 movements, L Finger-thumb 8.0 opposition, R Finger-thumb 8.0 opposition, L 26.0 Finger-nose test, R 18.0 Finger-nose test, L Sequencing of Complex Motor Acts 14.0 Fist-ring, R Fist-ring, L 8.0 Fist-edge-palm, R 24.0 14.0 Fist-edge-palm, L 23.0 Ozeretski 20.0 Rhythm tapping test, B Others Adventitious overflow test, R 8.0 Adventitious overflow test, L 8.0 Romberg test 0.0 Tremor, R 10.0 Tremor, L 14.0 Memory, 5 min 26.0 Memory, 10 min 30.0 48.0 Rhythm tapping test, A Mirror movements, R 56.0 Mirror movements, L 62.0 Synkinesis, R 30.0 Synkinesis, L 30.0 Convergence, R 10.0 Convergence, L 8.0 Gaze impersistence, R 2.0 2.0 Gaze impersistence, L Glabellar reflex 50.0 Snout reflex 0.0 8.0 Grasp reflex, R 0.0 Grasp reflex, L Suck reflex 12.0
0.10 -
0.749 -
0.05
0.822
Note. ICC = interclass correlation. A-V = audiovisual. R = right. L = left
(n
ICC = 46)
339 and 8 1% were receiving neuroleptics when examined. Controls consisted of 50 individuals with no history of psychiatric illness and were primarily drawn from the staff at the Maryland Psychiatric Research Center and other psychiatric facilities. The mean age was 32.1 years (SD = 8.1 years); 40% were male; and 50% were black. The two groups did not significantly differ in age or race, but there were significantly more males in the schizophrenic group than in the normal controls (~2 = 13.72, df = 1;p < 0.0002). Subjects in both groups were free of neurological or medical diseases thought likely to influence the test results. The schizophrenic patients were significantly more impaired than controls on total score and on all three functional areas of interest (see Table 2). On individual items, a higher proportion of schizophrenic patients than controls scored positively on 36 of the 41 items. Mean item scores were significantly higher in the schizophrenic patients for 20 items 0, < 0.05, two-tailed), with a trend toward significance @ < 0.10, two-tailed) in two others. Four additional items could not be statistically tested because there were no positive instances in the control group. Furthermore, three items which failed to show a significant difference were quite rare, occurring in < 10% of the schizophrenic patients. The remaining 12 items did not significantly differ between groups in spite of a reasonable rate of positive occurrence. Table 1 shows the rate of occurrence of each item by group and the results of an analysis of variance (ANOVA) by item. In each case, the ANOVA did or did not use the assumption of equal variance, depending on the results of the Levine test for equality of variance. Table 2. Neurological Evaluation Scale: Performance of schizophrenics controls on total score and functional areas of interest Schizophrenics (n = 98)
Controls (n = 50)
Mean
SD
Mean
SD
F
P
17.42
7.52
9.66
4.30
62.73
0.00001
Integration
4.11
2.35
2.68
1.77
14.32
0.0002
Coordination
1.94
1.42
0.78
0.91
36.15
0.00001
2.78
2.89
1.32
1.65
15.34
0.0001
Total score Sensory Motor
and
Sequencing of Complex Motor Acts
The effect of neuroleptics, age, sex, and race on the incidence of neurological signs in the two groups was examined. The effect of neuroleptics on neurological signs was evaluated in the context of an ongoing treatment study during which patients were sometimes drug free. Seventy-nine patients were on neuroleptics and 19 patients were drug free at the time of the examination. There were no significant differences between the two groups. Similarly, sex and age did not correlate significantly with scores on the instrument in either the schizophrenic or control subjects. However, race was significantly correlated, in the normal controls, with total score (r 0.43,~ = 0.002) and SI (r = 0.46, p < O.OOl), with greater impairment in the black controls (see Table 3). Similarly, in the schizophrenic patients, race was significantly correlated with total score (r 0.29,~ 0.004), SI (r = 0.27,~ 0.007), and SQ(r=0.35,p
q
q
q
340 Table 3. Effect of sex on incidence of neurological controls Blacks (n = 25)
signs in schizophrenics
Whites (n = 25)
Controls
Mean
SD
Mean
SD
F
Total score
11.52
4.71
7.80
3.12
10.84
<0.002
Sensory Integration
3.48
1.85
1.88
1.27
12.71
Motor Coordination
0.80
0.96
0.76
0.88
0.02
=0.88
Sequencing of Complex Motor Acts
1.48
1.83
1.16
1.46
0.47
=0.50
Blacks (n = 47)
P
Whites (n = 51)
Mean
SD
Mean
SD
F
19.87
7.87
15.16
6.46
10.58
<0.002
Sensory integration
4.76
2.45
3.51
2.12
7.39
co.008
Motor Coordination
1.81
1.28
1.90
1.51
0.11
=0.74
Sequencing of Complex Motor Acts
3.81
3.09
1.82
2.29
13.20
Schizophrenics Total score
and
P
=0.0005
black patients showing greater impairment than the white patients (see Table 3). However, an analysis of covariance (ANCOVA) controlling for race was conducted, and the significant difference between schizophrenic patients and controls for total score and the three functional areas of interest remained. A similar analytic approach was used to determine if the difference between black and white patients was related to medication status. An ANCOVA controlling for medication status demonstrated that the difference between black and white patients on total score and the three functional areas of interest was not due to medication status. The correlation between total score and each of the functional areas of interest was examined by calculating the Pearson r coefficients, to determine the interrelationship of the conceptual categories. The results are presented in Table 4. The three functional areas of interest are highly correlated with total score in both the patients and controls except for motor coordination in the control subjects, which is only moderately correlated with total score. The three functional areas of interest are not correlated with each other in the control subjects, and are moderately correlated with each other in the schizophrenic patients. Discussion The Neurological Evaluation Scale (NES) is a structured clinical evaluation designed complement the traditional neurological examination in assessing those neurological impairments that have been reported to have an increased prevalence in schizophrenia. It provides a total score, item score, and scores for three functional areas of interest thought to be conceptually meaningful. The battery is designed for ease of
to
341 Table 4. Correlation
between total score and each functional Total score
Controls (n = 50) Total score
Sensory Integration
Motor Coordination
Sequencing of Complex Motor Acts
-
Sensory Integration
0.661
-
Motor Coordination
0.342
0.10
-
Sequencing of Complex Motor Acts
0.541
0.17
0.06
Schizophrenics Total score
area of interest
-
(n = 96) -
Sensory Integration
0.681
Motor Coordination
0.571
0.263
-
Sequencing of Complex Motor Acts
0.691
0.313
0.263
-
1. p = 0.001.
2. p = 0.05. 3. p = 0.01. taking about 35 min to conduct and score, and requiring minimal can be scored in a highly reliable way, and clinician and nonclinician raters can be readily trained in its use. Schizophrenic patients differ significantly from controls on total score and the three functional areas of interest. This is consistent with previous studies comparing schizophrenic patients and nonpsychiatric controls (Kennard, 1960; Hertzig and Birch, 1966, 1968; Cox and Ludwig, 1979a, 1979b; Dimond et al., 1979; Weller and Kugler, 1979; Manschreck et al., 198la, 198lb, 1982; Walker and Green, 1982; Manschreck and Ames, 1984; Woods et al., 1986). In addition, the percentage of schizophrenic patients having a positive sign was higher than for controls on 36 of the 4 1 items, with the difference being significant for 20 items. However, on five items (e.g., graphesthesia (right), mirror movements (right and left), and glabellar and grasp (right) reflexes, the percentage of controls was greater, and on several other items (e.g., graphesthesia, right-left confusion, and mirror movements) a relatively high percentage of normals scored positively. The incidence of neurological signs in normal controls has been previously reported to be as low as 5% (Hertzig and Birch, 1966, 1968; Rochford et al., 1970; Manschreck and Ames, 1984). These incidences are in marked contrast with both our results and the > 50% incidence reported by others (Kennard, 1960; Cox and Ludwig, 1979b; Walker and Green, 1982). For individual items, there is little information from previous studies for comparison. Manschreck and Ames (1984) found no agraphesthesia in their patients, whereas Kennard (1960) found a 15% incidence, which was almost identical to that seen in the schizophrenic subjects. The differences in the incidence of neurological impairment are related in part to differences in the comprehensiveness of the assessment procedure and perhaps to differences in the
administration, equipment.
It
342 control groups. The differences on individual items may also be related to differences in the control groups and perhaps also to the sensitivity of the scoring guidelines used. Despite the differences in the range of incidences, there is consistent agreement that schizophrenic patients show more severe neurological impairment as reflected in their having more signs. A difficulty in any study comparing schizophrenic patients to normal controls is the difficulty in being blind to diagnosis. There is no simple solution to this problem. The consistency of the finding, across centers, of greater neurological impairment in schizophrenic patients (Heinrichs and Buchanan, 1988) and the findings in high-risk studies of greater neurological impairment in the offspring of schizophrenic parents (where the diagnosis of the child’s parents is unknown) (Marcus et al., 1985) argue against the difference being due to rater bias. In addition, there was no evidence in our study of the operation of the bias that the controls would be normal neurologically, as a significant number were rated as having more than one sign present. This does not preclude the presence of rater bias, as it may still have been operative in producing the group differences. Future studies could use video tapes of the subject’s examination to reduce the risk of rater bias derived from knowledge of the subject’s diagnosis. The effect of neuroleptics on neurological signs was evaluated by comparing drug-free schizophrenic patients to those on neuroleptics, as the current study was not specifically designed to evaluate the effect of neuroleptics on the incidence of neurological signs. There were no significant differences between the two groups. Previous studies examining the effect of neuroleptics on neurological signs in schizophrenic patients have also been between-group analyses. With one exception, they found no evidence of a neuroleptic effect (Quitkin et al., 1976; Cox and Ludwig, 19794 19796; Weller and Kugler, 1979; Manschreck et al., 1981a, 19796; Walker 1981; Walker and Green, 1982; Walker and Shaye, 1982). Quitkin et al. (1986) reported increased neurological signs in a group of schizophrenic patients whom they were unable to study drug free, as compared to schizophrenic patients who had been successfully studied drug free. It is unclear if the difference between the two groups represented a medication effect, or was related to differences in severity as exhibited by the ability to be kept drug free. The between-group comparison is only an indirect evaluation, as there may be important group differences (e.g., severity), in addition to the differences in drug status, which might explain the observed differences. A within-subject comparison, with subjects on and off neuroleptics, would be more informative on this important issue. Age and sex were not found to be correlated with total score or any of three functional areas of interest in either the normal controls or the schizophrenic patients. Previous studies have provided inconclusive results on the effect of age on neurological impairment (Heinrichs and Buchanan, 1988). The subjects in this study ranged in age from 20 to 55, so that the lack of relationship does not seem attributable to the limited age range of the group. The possibility of specific items being age dependent was not examined. Previous studies of sex-related differences have either found no difference or increased impairment in males (Heinrichs and Buchanan, 1988). The results from this study suggest that sex is not an important determinant of neurological impairment. Race was correlated with total score and SI in both the normal controls and the
343 schizophrenic patients, and with SQ in the patients. Although this finding is suggestive of a primary effect of race on the occurrence of neurological signs, the black and white controls and their schizophrenic counterparts may have differed on other important variables, resulting in the differences observed. This issue requires further study. When the effect of race was controlled, the difference between schizophrenic patients and normal controls remained. Each of the three functional areas of interest was significantly correlated with total score in the controls and patients, and with each other in the patients but not in the controls. The correlation between the different areas in schizophrenic patients is consistent with the presence of a general deficit (Chapman and Chapman, 1973), although it is possible that the intercorrelations represent a functional interdependence between the different areas or systems in the brain. By standardizing the administration and scoring of neurological impairment, the NES allows investigators in various centers to compare the results of neurological assessments. It is an inexpensive investigative tool and hence lends itself to application with large samples. Furthermore, any robust finding resulting from its use can be immediately applied in clinical settings. Using the NES, we have begun a series of investigations designed to answer many unsettled questions about clinically observable neurological signs in schizophrenia: Are these signs stable over time? Are they influenced by neuroleptic medication? Do they relate to the current clinical state of the patient? Are they useful as markers of subtypes of schizophrenia? Are they predictive of treatment response? Another area for future work is the clarification of the significance of these signsthat is, their neuroanatomical and neurophysiological correlates. Studies currently underway using the NES in brain imaging and electrophysiological investigations are a first step. A similar approach has recently been used to good advantage in relating neurological signs to positron emission tomography (PET) scan findings in Huntington’s disease (Young et al., 1986). The study of neurological signs in schizophrenia need not be “soft” and should take its place among those strategies being used to enhance the neuropsychiatric understanding of schizophrenia. Acknowledgment. The comments of William T. Carpenter, Jr., M.D., are gratefully acknowledged. The research reported was supported, in part, by grants MH-09044, MH-40279, and MH-35996 from the National Institute of Mental Health.
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Appendix.
Neurological
1. Tandem
Walk
Evaluation
Instructions: Subject to walk, in a straight
Scale
line, 12 feet, heel to toe.
Assessment: 0 = no missteps after subject has completed first full step; missteps after completion of first full step; 2 = 3 or more missteps, grabbing,
2. Romberg
1 = one or two or falling.
Test
Instructions: Subject to stand with his/her feet together, eyes closed, his/her arms held parallel to the floor, and fingers spread apart. The subject is to maintain this position for 1 min. Assessment: 0 = relatively stable, minimal swaying; maintain balance or falls.
3. Adventitious
I= marked swaying; 2 = subject steps to
Overflow
Instructions: Same as Romberg
Test.
Assessment: 0 = absence of movement of fingers, hands, or arms; 1 = irregular fluttering movement of fingers only; 2 = irregular fluttering movement extended to hands and/ or arms.
4. Tremor Instructions: Same as Romberg Assessment: 0 = no tremor;
Test.
1 = mild, fine tremor;
2 = marked,
fine or coarse tremor.
6. Cerebral Dominance a. Handedness Instructions: Ask subject to demonstrate how he/ she would write, throw a ball, use a tennis racket, strike a match, use scissors, thread a needle, use a broom, use a shovel, deal cards, use a hammer, brush teeth, and unscrew the lid of a jar. Assessment: R-Subject writes with right hand and performs at least seven other activities with right hand; M-Subject writes with right/left hand but performs less than seven other activities with right/left hand; L-Subject writes with left hand and performs at least seven other activities with left hand.
346 b. Footedness Instructions:
Ask subject to demonstrate
Assessment:
R-Subject
how he/she
would kick a ball.
kicks ball with right foot; L-Subject
kicks ball with left foot.
c. Eyedness instructions: Ask subject, with both eyes open, to look at a distant object through a hole in the center of a 3-inch x 5-inch index card that is held with both hands 18 inches in front of the subject. The subject is to close one eye at a time and tell the examiner with which eye closed did he/she lose sight of the object. Assessment: R-Subject loses sight of object with right eye closed; L-Subject of object with left eye closed.
7. Audio-Visual
loses sight
Integration
Instructions: The subject is asked to match a set of tapping sounds with one of three sets of dots presented on a 5-inch x 7-inch index card. The subject is instructed to close his/ her eyes during the tapping. Three practice trials are performed first to ensure that the subject understands the directions. Assessment:
0
q
no error;
1
one error; 2 = two or more errors.
q
8. Stereognosis Instructions: Subject, with eyes closed, is asked to identify an object placed in his/ her hand. Subject is instructed to feel the object with one hand and to take as much time as needed. If subject cannot name the object, he/she is asked to describe for what purpose the object is used. The subject starts with the dominant hand, based on the prior evaluation of handedness, or the hand with which he/she writes, if there is mixed hand dominance. The instructions are repeated at the beginning of the second trial. Assessment:
0
q
no errors;
1 = one error; 2 = more than one error.
9. Graphesthesia Instructions: Subject, with eyes closed, is asked to identify the number written on the tip of his/her forefinger. The order of hands is determined as with stereognosis. Assessment:
10.
Fist-Ring
0 = no errors;
1
q
one error;
2
q
more than one error.
Test
Instructions: The subject is asked to alternate placing his/her hand on the table, in the position of a fist, with the thumb placed either over the knuckles or over the middle phalanges and placing his/ her hand, on the table, in the position of a ring, with the tips of the thumb and forefinger touching and the remaining three fingers extended. The subject is to bring his/ her arm into the upright position between each change in hand position. If the subject does not perform the movement accurately or in a manner that can be appropriately assessed, he/ she is to be stopped, to be reinstructed, and to start the test again. The subject is to repeat each set of hand position changes 15 times.
347
Assessment: 0 = no major disruption of motion after first repetition; errors limited to incomplete extension of fingers in ring position and no more than two hesitancies in the transition from fist to ring or vice versa and no more than one fist/ ring confusion; 1q no major disruption of motion after first repetition or complete breakdown of motion; more than two hesitancies in the transition from fist to ring, difficulty in developing and maintaining a smooth, steady flow of movement, three to four fist/ring confusions, or any total of three but not more than four errors. 2 = major disruption of movement or complete breakdown of motion, or more than four fist Jring hesitations or confusions.
11. Fist-Edge-Palm
Test
Instructions: Ask the subject, using a smooth and steady rhythmic pattern, to touch the table with the side of his/ her fist, the edge of his/ her hand, and the palm of his/ her hand. The subject is to break contact with the surface of the table between each change in hand position, but not to bring the arm back in full flexion. The subject is to repeat this sequence of position changes 15 times. Assessment: 0 q no major disruption of motion afterfirst repetition; errors limited to no more than two hesitancies in the transition from one position to the next and no more than one mistake in hand position. 1 = no major disruption of motion after first repetition or complete breakdown of motion; more than two hesitancies in the transition from one position to another, difficulty in developing and maintaining a smooth, steady flow of movement, three to four position confusions, or any total of three or four errors. 2 = major disruption of movement or complete breakdown of motion, or more than four hesitations or position confusions. 12.
Ozeretski
Test
Instructions: The subject is to place both hands on the table, one hand palm down and the other hand in the shape of a fist. The subject is then asked simultaneously to alternate the position of his/her hands in a smooth and steady motion. The subject is asked to repeat this motion 15 times. Assessment: 0 q no major disruption of motion afterfirst repetition; errors limited to no more than two hesitancies in the transition from one position to the next and no more than one mistake in hand position. 1 = no major disruption of motion after first repetition or complete breakdown of motion; more than two hesitancies in the transition from one position to another, difficulty in developing and maintaining a smooth, steady flow of movement, three to four position confusions, or any total of three, but no more than four errors. 2 = major disruption of movement or complete breakdown of motion, or more than four hesitations or position confusions.
13. Memory Instructions: Subject is told four words and is asked to repeat them immediately after they are all presented. If the subject is unable to repeat the four words correctly, they are represented. If the subject still cannot repeat the four words after a total of three presentations of the words, the test is terminated and the subject is given a score of 2 for both parts of the item. If the subject is able to repeat the four words after the initial or two subsequent presentations, he/she is then asked to remember the words as well as possible and told that he/ she will be asked to repeat the words twice later on during the interview. The subject is then asked to recall the four words at 5 and 10 min. Assessment: 0 = Subject remembers all words; Subject remembers fewer than three words.
1 = Subject
remembers
three words; 2
q
348
14. Rhythm Tapping Test Part A instructions: Ask the subject to reproduce exactly the series of taps heard while the subject has eyes closed. The subject may have eyes open while reproducing series of taps. Assessment: 0 = no errors; I = one error of either nondiscrimination between soft and hard sounds, rhythm, or error in number of taps; 2 = more than one error.
Part B Instructions: Ask the subject Assessment: 0 = no errors;
to produce
a series of taps as instructed.
1 = one error; 2 = more than one error.
15. Rapid Alternating Movements Instructions: Ask the subject to place his/ her hands palm down on legs. The subject is to start with his/ her dominant hand and is to slap his/ her leg distinctly with the palm and the back of his/ her hand in an alternating motion. The determination of dominance is as described above (see item 8). The subject is to perform the task 20 times, with both hands, one hand at a time. Assessment: 0 q no major disruption of motion, hesitation, or mistake in hand placement; I of motion or one to two hesitations or mistakes in hand placement; 2 = major disruption of motion or three or more hesitations or mistakes in hand placement.
= no major disruption
16. Finger-Thumb Opposition Instructions: Ask the subject to place both hands palm up with fingers fully extended on his/ her legs. The subject is to start with his/ her dominant hand and is to touch the tip of his/ her fingers with the tip of his/her thumb, from forefinger to pinky, returning to forefinger, for a total of IO repetitions. Assessment: 0 = no major disruption of motion and no more than one mistake; I = no major disruption of motion or two to three mistakes; 2 = major disruption of motion or four or more mistakes.
17. Mirror Movements Instructions: The subject’s hand, which is not performing the Finger-Thumb Test, is observed for parallel movements of the fingers and thumb. Assessment: 0 = no observable repetitive movements of the fingers;
Opposition
movements of the fingers; I = minor, inconsistent, 2 = consistent, distinctive movements of the fingers.
or
18. Extinction (Face-Hand Test) Instructions: The subject is seated, with hands resting palm down, on his/her knees and with eyes closed. The subject is told that he/she will be touched on either the cheek, hand, or both, and is to say where he/she has been touched. If the subject names just one touch, he/she is asked-the first time this occurs only-if he/she felt a touch anywhere else. The simultaneous touching is done in the following order: right cheek-left hand, left cheek-right hand, right cheek-right hand, left cheek-left hand, both hands, and both cheeks.
349 Assessment:
0 = no errors;
20. Right/Left
1 = one error; 2 = more than one error.
Confusion
Instructions: Subject is asked to point to his/her right foot, left hand; place his/her right hand to left shoulder, left hand to right ear; point to examiner’s left knee, right elbow; with examiner’s arms crossed, point to examiner’s left hand with his/ her right hand, and with examiner recrossing arms, point to examiner’s right hand with his] her left hand. Assessment:
0
q
no errors;
1 = one error; 2 = two or more errors.
21. Synkinesis Instructions: Subject is instructed to follow the cap of a pen with his/ her eyes only as it is moved between extremes of horizontal gaze. If the subject moves his/ her head, the subject is asked to keep his/ her head still and follow the cap of a pen with the eyes only. Assessment: when specifically still.
0 = no movement of the head; 1 = movement of the head on first trial but not told to keep head still; 2 = movement of the head even when told to keep head
22. Convergence Instructions: Subject is instructed toward the subject’s nose.
to follow the cap of a pen with his/ her eyes as it is moved
Assessment: 0 = both eyes converge on object; 1 = one or both eyes are unable to converge completely, but can converge more than halfway; 2~ one or both eyes fail to converge more than halfway.
23. Gaze lmpersistence Instructions: Subject is instructed to fix his/ her gaze on the cap of a pen at a 45 o angle in the horizontal plane of the right and left visual fields for 30 sec. Assessment: 0 = no deviation from fixation; deviation from fixation before 20 sec.
1 = deviation
from fixation
after 20 set; 2 =
24. Finger to Nose Test Instructions: The subject is instructed tip of his/ her index finger.
to close eyes and touch the tip of his/ her nose with the
Assessment: 0 = no intention tremor or passpointing; pointing; 2 = marked intention tremor or passpointing.
25. Glabellar
1 = mild intention
tremor
or pass-
Reflex
Instructions: Subject is instructed to fix his/ her gaze on a point across the room. The subject is approached from above the forehead outside of the visual field, and the examiner taps the glabellar region 10 times with the index finger. Assessment: 0 = three or fewer blinks; 1 = four or five full blinks, or more than six partial or full blinks; 2 = six or more full blinks.
350 26. Snout
Reflex
Instructions: Subject is instructed subject’s philtrum.
to relax, and the examiner
presses his finger against the
Assessment: 0 = no contraction of the orbicularis orris (or puckering contraction of the orbicularis orris (or puckering of the lips).
of the lips); 2 = any
27. Grasp Reflex Instructions: The subject is instructed not to grab, and the examiner strokes the inside of the subject’s palm between the index finger and thumb. This procedure is repeated a second time with the subject being asked to spell the word “help” backwards. Assessment: 0 = no flexion of the subject’s fingers; 1= mild flexion of the subject’s fingers on first trial or flexion of any kind on second trial; 2 q marked flexion of the subject’s fingers on first trial.
28. Suck Reflex Instructions: The examiner between the subject’s lips. Assessment:
places the knuckle of a flexed index finger or tongue depressor
0 = no movement;
2
q
any pursing
or sucking
motion
by the subject’s lips.
Psyc.hiatr_yResearch. 21,335-350 Elsevier
The Neurological Evaluation Scale (NES): A Structured Instrument for the Assessment of Neurological Signs in Schizophrenia Robert W. Buchanan
and Douglas
W. Heinrichs
Received January 22, 1988; revised version received August 17, 1988; accepted September 1988.
19.
Abstract. The significance of neurological signs in schizophrenia is poorly understood. In part, this may reflect the marked variability in the methods of ascertainment in previous studies. The Neurological Evaluation Scale (NES) is designed to standardize the assessment of neurological impairment in schizophrenia. The battery consists of 26 items. Data on the interrater reliability for total score, functional areas of interest, and individual items are presented. Preliminary validity data demonstrate the abiIity of the battery to discriminate patients with schizophrenia from nonpsychiatric controls. Key Words. Neurological
signs, assessment,
schizophrenia.
During the last two decades there has been a growing appreciation of the biological underpinnings of most major psychiatric syndromes including schizophrenia. This coincides with a major reawakening of interest in clinical problems at the interface of psychiatry and neurology, as reflected in the terms “neuropsychiatry” and “behavioral neurology” (Pincus and Tucker, 1974; Cummings, 1985; Mesulam, 1985; Hales and Yudofsky, 1987). In part, this is a response to the profound impact of psychotropic medication on the course of these disorders, but the availability of ever more sophisticated techniques for the biochemical, anatomical, and physiological examination of the brain has been a pivotal factor. In particular, advances in brain imaging have stimulated efforts to characterize the neuropathology of schizophrenia, and the “neurology of schizophrenia” has drawn increased research interest (Henn and Nasrallah, 1982; Andreasen, 1986; Nasrallah and Weinberger, 1986). Imaging studies have largely concentrated on image quantification, but there is a need for precise behavioral and clinical assessments to interpret these findings (Roland et al., 1987), including careful attention to the clinical manifestations of the neurological processes that accompany schizophrenic disorders. There is a long history, in schizophrenia, of anecdotal reports and descriptions of abnormalities on clinical neurological examination. In the past 25 years, a number of systematic surveys and controlled studies of neurological abnormalities have appeared in the literature. In reviewing this literature (Heinrichs and Buchanan, 1988), we found 19 studies that allowed comparisons between patients with schizophrenia
Robert W. Buchanan, M.D., and Douglas W. Heinrichs, M.D., are Assistant Professors of Psychiatry, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD. (Reprint requests to Dr. R.W. Buchanan, USA.) 0165-I 78 I /89/%03.50
Maryland
Psychiatric
@ 1989 Elsevier Scientific
Research
Publishers
Center,
Ireland
P.O. Box 21247, Baltimore,
Ltd.
MD 21228,
336 and controls. Without exception, there was an increased prevalence of neurological signs in schizophrenic patients compared to nonpsychiatric controls, and in most studies more neurological abnormalities were present in schizophrenic patients than in mixed diagnostic and affective disorder groups. Furthermore, evidence suggests that neurological abnormalities may relate to symptom dimensions, course of illness, and family history of schizophrenia, as well as being present in individuals at high risk before the onset of their illness (Heinrichs and Buchanan, 1988). Yet, for all this, abnormal neurological signs have received relatively little attention from investigators or clinicians. This neglect may stem, in part, from the belief that these findings are ambiguous, unreal, fleeting, nonreproducible, nonlocalizing, and uninterpretable-a viewpoint reflected in the frequent designation of these findings as “neurological soft signs.” However, our failure to understand the meaning of neurological symptoms in schizophrenia is probably more reflective of a limitation in our knowledge than a “softness” in the findings themselves. If neurological signs are to be an object of serious investigation, then precise and reproducible methods of assessment are needed. There is tremendous variability among existing studies in how signs are elicited and rated, and for many reports the exact methods are not described (Heinrichs and Buchanan, 1988). Many studies simply refer to a “comprehensive neurological examination.” Those studies that do specify methods tend to be the ones that focus on a specific and limited area of neurological abnormality. Less than half of the existing studies even mention reliability, though reliability coefficients, when evaluated, are usually quite acceptable. However, only one study has described a detailed and rigorous reliability exercise (Quitkin et al., 1976). Other important questions, such as temporal stability, practice effect, effect of medication, and impact of current clinical state, have not been adequately addressed. In this report, we present a structured neurological examination that addresses the areas of neurological impairment that have been consistently found in schizophrenia, a demonstration of the reliability of the examination, and preliminary data on its validity.
Construction of the Instrument A thorough search of the English-language literature focused on systematic surveys and controlled studies of clinical neurological evaluations of adult and adolescent patients with schizophrenia (Heinrichs and Buchanan, 1988). Specific signs representing areas of frequent impairment noted across multiple studies were selected. Dysfunction in three functional areas of interest (based on conceptual considerations of neuroanatomy and function) emerged from the review: 1. Integrative sensory dysfunction, reflected in items such as bilateral extinction, agraphesthesia, astereognosis, right/ left confusion, and impaired audiovisual integration. 2. Motor incoordination, reflected in items such as tandem walk, finger to nose, finger to thumb opposition, and dysdiadochokinesis. 3. Impaired sequencing of complex motor acts, reflected in items such as those used by Luria (1966), including the fist-ring, fist-edge-palm, and Ozeretski tests. In addition, abnormalities in eye movements (Stevens, 1982), frontal release signs (COX and Ludwig, 1979), and short-term memory (Broga and Neufield, 1981) have been frequently
337 observed. In contrast, primary sensory modalities, motor strength, and reflexes were characteristically intact in the schizophrenia cohorts previously studied (Heinrichs and Buchanan, 1988). From these considerations a battery of 26 discrete items, of which 14 items are tested and scored separately for the right and left sides of the body, was assembled. The instrument includes representative items from the three functional areas of interest, plus the assessment of cerebral dominance, short-term memory, frontal release signs, and eye movement abnormalities. All items are judged to be easily administered by a clinician at the bedside or in a consulting room with minimal equipment needed. A fixed order of administration is devised relating to ease of administration rather than conceptual categories. The procedure for administering each item is specified and standardized. Each item is scored on a 3-point scale: 0 = no abnormality; 1q mild, but definite impairment; and 2 = marked impairment, except for the snout and suck reflexes which are scored either as a 0 or 2. Descriptive anchors are provided for each score to facilitate standardized judgments (see Appendix). In addition to item scores and total score (sum of all items), subsets of items are totaled to yield scores for the three functional areas of interest discussed above: sensory integration, motor coordination, and sequencing of complex motor acts. The validity of these categories awaits further empirical assessment, and other categories may emerge from future analytic or conceptual approaches.
Reliability assess the interrater reliability using the battery, the authors simultaneously examined 46 subjects. Thirty-nine of the subjects were patients with a diagnosis of either DSM-III schizophrenia or schizophreniform disorder (American Psychiatric Association, 1980) or Research Diagnostic Criteria (RDC) schizoaffective, mainly schizophrenic disorder (Spitzer et al., 1978), and seven were normal controls. The raters scored the battery independently, alternating which rater conducted the examination. The interclass correlations for total score were 0.95; for sensory integration (SI), 0.99; for motor coordination (MC), 0.71; and for sequencing of complex motor acts (SQ), 0.89. Interclass correlations for each item are shown on Table 1. The interclass correlations were 2 0.90 for 14 items, 0.80-0.89 for 9 items, 0.70-0.79 for 7 items, 0.60-0.69 for 5 items, 0.50 to 0.59 for 3 items, and <0.50 for 3 items. The last three were rarer items, each occurring in < 10% of subjects. To determine the ability to train others to use the instrument reliably, one of the authors (R.W.B.) trained a nurse and a nonclinician research assistant and then conducted a reliability study with each. The reliability studies were conducted in the same manner as described for the two authors. Training, including the reliability exercise, took approximately 20 hours in each case. For the nurse, the interclass correlations for total score, SI, MC, and SQ, based on the examination of 15 subjects, were 0.88, 0.97, 0.72, and 0.80. The respective interclass correlations for the research assistant, based on the examination of 14 subjects, were 0.90, 0.98, 0.75, and 0.80.
To
Validity As a first step in the assessment of the validity of the instrument, we examined its ability to differentiate between schizophrenic outpatients and nonpatient controls. All of the subjects were examined by one of the authors. The patient group comprised 98 patients with either DSM-III schizophrenia or schizophreniform disorder or RDC schizoaffective disorder, mainly schizophrenic. The mean duration of illness was 8.4 years. The mean age was 32.1 years (SD = 8.3 years); 71% were male; 47% were black;
338 Table 1. Neurological Evaluation Scale: Interclass correlations for each item % with positive sign Item
Controls
Schizophrenics
(n = 50)
(n = 98)
F
P
72.4 7.1 14.3 42.8 46.9 19.4 74.5
28.00 2.75 5.49 0.02 1.92 -
0.00001 0.01 0.02 0.89 0.168 -
0.50
0.482
1.00 1.00 0.95 1.00 1.00 1.00 0.93
18.4
9.35
0.003
0.87
4.1
0.07
0.795
1 .oo
13.2
2.00
0.160
0.57
8.2
0.14
0.681
0.77
18.4 49.0 44.9
4.66 9.39 16.42
0.032 0.0003 0.0001
0.77 0.80 0.72
31.6 28.6 41.8 29.6 37.8 31.6
7.75 11.94 6.66 9.03 2.93 2.53
0.006 0.0007 0.011 0.003 0.089 0.114
0.73 0.67 0.69 0.88 0.95 0.83
27.6
11..09
0.001
0.85
30.6 7.1 24.5 29.6 59.2 61.2 85.7 38.8 41.8 43.9 43.9 18.4 20.4 12.2 15.3 49.0 1.0 7.1 8.2 13.3
14.51 -
0.0002 -
3.55 4.29 32.77 25.06 34.58 1.53 2.49 2.18 1.75 1.95 7.60 8.68 8.17 0.78 -
0.062 0.04 0.00001 0.00001 0.00001 0.218 0.017 0.142 0.188 0.165 0.007 0.004 0.005 0.378 -
0.81 0.88 0.58 0.64 0.94 0.99 0.97 0.56 0.75 0.90 0.72 0.67 0.77 0.86 0.95 0.81 0.0 0.44 0.14 0.60
Sensory Integration 28.0 A-V integration 2.0 Stereognosis, R 4.0 Stereognosis, L 46.0 Graphesthesia, R 38.0 Graphesthesia, L 0.0 Extinction 64.0 R/L confusion Motor Coordination 4.0 Tandem walk Rapid alternating 4.0 movements, R Rapid alternating 4.0 movements, L Finger-thumb 8.0 opposition, R Finger-thumb 8.0 opposition, L 26.0 Finger-nose test, R 18.0 Finger-nose test, L Sequencing of Complex Motor Acts 14.0 Fist-ring, R Fist-ring, L 8.0 Fist-edge-palm, R 24.0 14.0 Fist-edge-palm, L 23.0 Ozeretski 20.0 Rhythm tapping test, B Others Adventitious overflow test, R 8.0 Adventitious overflow test, L 8.0 Romberg test 0.0 Tremor, R 10.0 Tremor, L 14.0 Memory, 5 min 26.0 Memory, 10 min 30.0 48.0 Rhythm tapping test, A Mirror movements, R 56.0 Mirror movements, L 62.0 Synkinesis, R 30.0 Synkinesis, L 30.0 Convergence, R 10.0 Convergence, L 8.0 Gaze impersistence, R 2.0 2.0 Gaze impersistence, L Glabellar reflex 50.0 Snout reflex 0.0 8.0 Grasp reflex, R 0.0 Grasp reflex, L Suck reflex 12.0
0.10 -
0.749 -
0.05
0.822
Note. ICC = interclass correlation. A-V = audiovisual. R = right. L = left
(n
ICC = 46)
339 and 8 1% were receiving neuroleptics when examined. Controls consisted of 50 individuals with no history of psychiatric illness and were primarily drawn from the staff at the Maryland Psychiatric Research Center and other psychiatric facilities. The mean age was 32.1 years (SD = 8.1 years); 40% were male; and 50% were black. The two groups did not significantly differ in age or race, but there were significantly more males in the schizophrenic group than in the normal controls (~2 = 13.72, df = 1;p < 0.0002). Subjects in both groups were free of neurological or medical diseases thought likely to influence the test results. The schizophrenic patients were significantly more impaired than controls on total score and on all three functional areas of interest (see Table 2). On individual items, a higher proportion of schizophrenic patients than controls scored positively on 36 of the 41 items. Mean item scores were significantly higher in the schizophrenic patients for 20 items 0, < 0.05, two-tailed), with a trend toward significance @ < 0.10, two-tailed) in two others. Four additional items could not be statistically tested because there were no positive instances in the control group. Furthermore, three items which failed to show a significant difference were quite rare, occurring in < 10% of the schizophrenic patients. The remaining 12 items did not significantly differ between groups in spite of a reasonable rate of positive occurrence. Table 1 shows the rate of occurrence of each item by group and the results of an analysis of variance (ANOVA) by item. In each case, the ANOVA did or did not use the assumption of equal variance, depending on the results of the Levine test for equality of variance. Table 2. Neurological Evaluation Scale: Performance of schizophrenics controls on total score and functional areas of interest Schizophrenics (n = 98)
Controls (n = 50)
Mean
SD
Mean
SD
F
P
17.42
7.52
9.66
4.30
62.73
0.00001
Integration
4.11
2.35
2.68
1.77
14.32
0.0002
Coordination
1.94
1.42
0.78
0.91
36.15
0.00001
2.78
2.89
1.32
1.65
15.34
0.0001
Total score Sensory Motor
and
Sequencing of Complex Motor Acts
The effect of neuroleptics, age, sex, and race on the incidence of neurological signs in the two groups was examined. The effect of neuroleptics on neurological signs was evaluated in the context of an ongoing treatment study during which patients were sometimes drug free. Seventy-nine patients were on neuroleptics and 19 patients were drug free at the time of the examination. There were no significant differences between the two groups. Similarly, sex and age did not correlate significantly with scores on the instrument in either the schizophrenic or control subjects. However, race was significantly correlated, in the normal controls, with total score (r 0.43,~ = 0.002) and SI (r = 0.46, p < O.OOl), with greater impairment in the black controls (see Table 3). Similarly, in the schizophrenic patients, race was significantly correlated with total score (r 0.29,~ 0.004), SI (r = 0.27,~ 0.007), and SQ(r=0.35,p
q
q
q
340 Table 3. Effect of sex on incidence of neurological controls Blacks (n = 25)
signs in schizophrenics
Whites (n = 25)
Controls
Mean
SD
Mean
SD
F
Total score
11.52
4.71
7.80
3.12
10.84
<0.002
Sensory Integration
3.48
1.85
1.88
1.27
12.71
Motor Coordination
0.80
0.96
0.76
0.88
0.02
=0.88
Sequencing of Complex Motor Acts
1.48
1.83
1.16
1.46
0.47
=0.50
Blacks (n = 47)
P
Whites (n = 51)
Mean
SD
Mean
SD
F
19.87
7.87
15.16
6.46
10.58
<0.002
Sensory integration
4.76
2.45
3.51
2.12
7.39
co.008
Motor Coordination
1.81
1.28
1.90
1.51
0.11
=0.74
Sequencing of Complex Motor Acts
3.81
3.09
1.82
2.29
13.20
Schizophrenics Total score
and
P
=0.0005
black patients showing greater impairment than the white patients (see Table 3). However, an analysis of covariance (ANCOVA) controlling for race was conducted, and the significant difference between schizophrenic patients and controls for total score and the three functional areas of interest remained. A similar analytic approach was used to determine if the difference between black and white patients was related to medication status. An ANCOVA controlling for medication status demonstrated that the difference between black and white patients on total score and the three functional areas of interest was not due to medication status. The correlation between total score and each of the functional areas of interest was examined by calculating the Pearson r coefficients, to determine the interrelationship of the conceptual categories. The results are presented in Table 4. The three functional areas of interest are highly correlated with total score in both the patients and controls except for motor coordination in the control subjects, which is only moderately correlated with total score. The three functional areas of interest are not correlated with each other in the control subjects, and are moderately correlated with each other in the schizophrenic patients. Discussion The Neurological Evaluation Scale (NES) is a structured clinical evaluation designed complement the traditional neurological examination in assessing those neurological impairments that have been reported to have an increased prevalence in schizophrenia. It provides a total score, item score, and scores for three functional areas of interest thought to be conceptually meaningful. The battery is designed for ease of
to
341 Table 4. Correlation
between total score and each functional Total score
Controls (n = 50) Total score
Sensory Integration
Motor Coordination
Sequencing of Complex Motor Acts
-
Sensory Integration
0.661
-
Motor Coordination
0.342
0.10
-
Sequencing of Complex Motor Acts
0.541
0.17
0.06
Schizophrenics Total score
area of interest
-
(n = 96) -
Sensory Integration
0.681
Motor Coordination
0.571
0.263
-
Sequencing of Complex Motor Acts
0.691
0.313
0.263
-
1. p = 0.001.
2. p = 0.05. 3. p = 0.01. taking about 35 min to conduct and score, and requiring minimal can be scored in a highly reliable way, and clinician and nonclinician raters can be readily trained in its use. Schizophrenic patients differ significantly from controls on total score and the three functional areas of interest. This is consistent with previous studies comparing schizophrenic patients and nonpsychiatric controls (Kennard, 1960; Hertzig and Birch, 1966, 1968; Cox and Ludwig, 1979a, 1979b; Dimond et al., 1979; Weller and Kugler, 1979; Manschreck et al., 198la, 198lb, 1982; Walker and Green, 1982; Manschreck and Ames, 1984; Woods et al., 1986). In addition, the percentage of schizophrenic patients having a positive sign was higher than for controls on 36 of the 4 1 items, with the difference being significant for 20 items. However, on five items (e.g., graphesthesia (right), mirror movements (right and left), and glabellar and grasp (right) reflexes, the percentage of controls was greater, and on several other items (e.g., graphesthesia, right-left confusion, and mirror movements) a relatively high percentage of normals scored positively. The incidence of neurological signs in normal controls has been previously reported to be as low as 5% (Hertzig and Birch, 1966, 1968; Rochford et al., 1970; Manschreck and Ames, 1984). These incidences are in marked contrast with both our results and the > 50% incidence reported by others (Kennard, 1960; Cox and Ludwig, 1979b; Walker and Green, 1982). For individual items, there is little information from previous studies for comparison. Manschreck and Ames (1984) found no agraphesthesia in their patients, whereas Kennard (1960) found a 15% incidence, which was almost identical to that seen in the schizophrenic subjects. The differences in the incidence of neurological impairment are related in part to differences in the comprehensiveness of the assessment procedure and perhaps to differences in the
administration, equipment.
It
342 control groups. The differences on individual items may also be related to differences in the control groups and perhaps also to the sensitivity of the scoring guidelines used. Despite the differences in the range of incidences, there is consistent agreement that schizophrenic patients show more severe neurological impairment as reflected in their having more signs. A difficulty in any study comparing schizophrenic patients to normal controls is the difficulty in being blind to diagnosis. There is no simple solution to this problem. The consistency of the finding, across centers, of greater neurological impairment in schizophrenic patients (Heinrichs and Buchanan, 1988) and the findings in high-risk studies of greater neurological impairment in the offspring of schizophrenic parents (where the diagnosis of the child’s parents is unknown) (Marcus et al., 1985) argue against the difference being due to rater bias. In addition, there was no evidence in our study of the operation of the bias that the controls would be normal neurologically, as a significant number were rated as having more than one sign present. This does not preclude the presence of rater bias, as it may still have been operative in producing the group differences. Future studies could use video tapes of the subject’s examination to reduce the risk of rater bias derived from knowledge of the subject’s diagnosis. The effect of neuroleptics on neurological signs was evaluated by comparing drug-free schizophrenic patients to those on neuroleptics, as the current study was not specifically designed to evaluate the effect of neuroleptics on the incidence of neurological signs. There were no significant differences between the two groups. Previous studies examining the effect of neuroleptics on neurological signs in schizophrenic patients have also been between-group analyses. With one exception, they found no evidence of a neuroleptic effect (Quitkin et al., 1976; Cox and Ludwig, 19794 19796; Weller and Kugler, 1979; Manschreck et al., 1981a, 19796; Walker 1981; Walker and Green, 1982; Walker and Shaye, 1982). Quitkin et al. (1986) reported increased neurological signs in a group of schizophrenic patients whom they were unable to study drug free, as compared to schizophrenic patients who had been successfully studied drug free. It is unclear if the difference between the two groups represented a medication effect, or was related to differences in severity as exhibited by the ability to be kept drug free. The between-group comparison is only an indirect evaluation, as there may be important group differences (e.g., severity), in addition to the differences in drug status, which might explain the observed differences. A within-subject comparison, with subjects on and off neuroleptics, would be more informative on this important issue. Age and sex were not found to be correlated with total score or any of three functional areas of interest in either the normal controls or the schizophrenic patients. Previous studies have provided inconclusive results on the effect of age on neurological impairment (Heinrichs and Buchanan, 1988). The subjects in this study ranged in age from 20 to 55, so that the lack of relationship does not seem attributable to the limited age range of the group. The possibility of specific items being age dependent was not examined. Previous studies of sex-related differences have either found no difference or increased impairment in males (Heinrichs and Buchanan, 1988). The results from this study suggest that sex is not an important determinant of neurological impairment. Race was correlated with total score and SI in both the normal controls and the
343 schizophrenic patients, and with SQ in the patients. Although this finding is suggestive of a primary effect of race on the occurrence of neurological signs, the black and white controls and their schizophrenic counterparts may have differed on other important variables, resulting in the differences observed. This issue requires further study. When the effect of race was controlled, the difference between schizophrenic patients and normal controls remained. Each of the three functional areas of interest was significantly correlated with total score in the controls and patients, and with each other in the patients but not in the controls. The correlation between the different areas in schizophrenic patients is consistent with the presence of a general deficit (Chapman and Chapman, 1973), although it is possible that the intercorrelations represent a functional interdependence between the different areas or systems in the brain. By standardizing the administration and scoring of neurological impairment, the NES allows investigators in various centers to compare the results of neurological assessments. It is an inexpensive investigative tool and hence lends itself to application with large samples. Furthermore, any robust finding resulting from its use can be immediately applied in clinical settings. Using the NES, we have begun a series of investigations designed to answer many unsettled questions about clinically observable neurological signs in schizophrenia: Are these signs stable over time? Are they influenced by neuroleptic medication? Do they relate to the current clinical state of the patient? Are they useful as markers of subtypes of schizophrenia? Are they predictive of treatment response? Another area for future work is the clarification of the significance of these signsthat is, their neuroanatomical and neurophysiological correlates. Studies currently underway using the NES in brain imaging and electrophysiological investigations are a first step. A similar approach has recently been used to good advantage in relating neurological signs to positron emission tomography (PET) scan findings in Huntington’s disease (Young et al., 1986). The study of neurological signs in schizophrenia need not be “soft” and should take its place among those strategies being used to enhance the neuropsychiatric understanding of schizophrenia. Acknowledgment. The comments of William T. Carpenter, Jr., M.D., are gratefully acknowledged. The research reported was supported, in part, by grants MH-09044, MH-40279, and MH-35996 from the National Institute of Mental Health.
References American Psychiatric Association. DSM-III: Diagnostic and Statistical Manual of Mental Disorders. 3rd ed. Washington, DC: APA, 1980. Andreasen, N.C., ed. Can Schizophrenia be Localized in the Brain? Washington, DC: American Psychiatric Press, Inc., 1986. Broga, M.I., and Neutield, R.W.J. Evaluation of information sequential aspects of schizophrenic performance: I. Framework and current findings. Journal of Nervous and Mental Disease, 169:558-568, 1981. Chapman, L.J., and Chapman, J.P. Disordered nought in Schizophrenia. New York: Appleton-Century-Crofts, 1973. Cox, SM., and Ludwig, A.M. Neurological soft signs and psychopathology: Findings in schizophrenia. Journal of Nervous and Mental Disease, 167:161-165, 1979a.
344
Cox, SM., and Ludwig, A.M. Neurological soft signs and psychopathology: Incidence in diagnostic groups. Canadian Journal of Psychiatry, 24:668-673, 19796. Cummings, J.L. Clinical Neuropsychiatry. Orlando, FL: Grune 8~ Stratton, Inc., 1985. Dimond, S.S.J.; Scammell, R.E.; Pryce, I.G.; Haus, D.; and Gray, C. Callosal transfer and left-hand anomia in schizophrenia. Biological Psychiatry, 14735-739, 1979. Hales, H.E., and Yudofsky, SC., eds. Textbook of Neuropsychiatry. Washington, DC: American Psychiatric Press, Inc., 1987. Heinrichs, D. W., and Buchanan, R.W. The significance and meaning of neurological signs in schizophrenia. American Journal of Psychiatry, 145: 1I-18, 1988. Henn, F.A., and Nasrallah, H.A., eds. Schizophrenia as a Brain Disease. New York: Oxford University Press, Inc., 1982. Hertzig, M.E., and Birch. H.G. Neurologic organization in psychiatrically disturbed adolescent girls. Archives of General Psychiatry, 15:590-598, 1966. Hertzig, M.E., and Birch, H.G. Neurologic organization in psychiatrically disturbed adolescents. Archives of Genera/ Psychiatry, 19528-537, 1968. Kennard, M.A. Value of equivocal signs in neurologic diagnosis. Neurology, 10:753-754, 1960. Luria, A.R. Higher Cortical Functions in Man. New York: Basic Books, 1966. Manschreck, T.C., and Ames, D. Neurologic features and psychopathology. Biological Psychiatry,
19:703-719,
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Manschreck, T.C.; Maher, B.A.; and Ader, D.N. Formal thought disorder, the type-token ratio, and disturbed voluntary motor movement in schizophrenia. British Journal ofpsychiatry, 139:7-15, 198la. Manschreck, T.C.; Maher, B.A.; Rucklos, M.E.; Vereen, D.R.; and Ader, D.N. Deficient motcr synchrony in schizophrenia. Journal of Abnormal Psychology, 90:321-328, 198lb. Manschreck, T.C.; Maher, B.A.; Rucklos, M.E.; and Vereen, D.R. Disturbed voluntary motor activity in schizophrenic disorder. Psychological Medicine, 12:73-84, 1982. Marcus, J.; Hans, S.L.; Lewow, E.; Wilkinson, L.; and Burack, C.M. Neurological findings in high-risk children. Schizophrenia Bulletin, 11:85-100, 1985. Mesulam, M.M.. ed. Principles of Behavioral Neurology. Philadelphia, PA: F.A. Davis Company, 1985. Nasrallah, H.A., and Weinberger, D.R., eds. Handbook of Schizophrenia: The Neurology of Schizophrenia. Vol. 1. Amsterdam: Elsevier Science Publishers, 1986. Pincus, J.H., and Tucker, G.J. Behavioral Neurology. 3rd ed. New York: Oxford University Press, 1974. Quitkin, F.; Rifkin, A.; and Klein, D.F. Neurologic soft signs in schizophrenia and character disorders. Archives of General Psychiatry, 33:845-853, 1976. Rochford, M.D.; Detre, T.; Tucker, G.J.; and Harrow, M. Neuropsychological impairments in functional psychiatric diseases. Archives of General Psychiatry, 22: 114-l 19, 1970. Roland, P.E.; Eriksson, L.; Stone-Elander, S.; and Widen, L. Does mental activity change the oxidative metabolism of the brain? Journal of Neuroscience, 712372-2389, 1987. Spitzer, R.L.; Endicott, J.; and Robins, E. Research Diagnostic Criteria: Rationale and reliability. Archives of General Psychiatry, 35~773-782, 1978. Stevens, J.R. Neurology and neuropathology of schizophrenia. In: Henn, F.A., and Nasrallah, H.A., eds. Schizophrenia as a Brain Disease. New York: Oxford University Press, Inc., 1982. pp. 112-147. Walker, E. Attentional and neuromotor functions of schizophrenics, schizoaffectives, and patients with other affective disorders. Archives of General Psychiatry, 38:1355-1358, 1981. Walker, E., and Green, M. Soft signs of neurological dysfunction in schizophrenia: An investigation of lateral performance. Biological Psychiatry, 17:381-386, 1982. Walker, E., and Shaye, J. Familial schizophrenia: A predictor of neuromotor and attentional abnormalities in schizophrenia. Archives of General Psychiatry, 39: 1153-I 156, 1982. Weller, M., and Kugler, B.T. Tactile discrimination in schizophrenic and affective psychoses. In: Gruzelier, J., and Flor-Henry, P., eds. Hemispheric Asymmetries of Function in Psychopathology. Amsterdam: Elsevier/ North-Holland Biomedical Press, 1979.
345 Woods, B.T.; Kinney, D.K.; and Yurgelun-Todd, D. Neurologic abnormalities in schizophrenic patients and their families: I. Comparison of schizophrenic, bipolar, and substance abuse patients and normal controls. Archives of General Psychiatry, 43:657-663, 1986. Young, A.B.; Penney, J.B.; Starosta-Rubinstein, S.; Markel, D.S.; Berent, S.; Giordani, B.; Ehrenkaufer, R.; Jewett, D.; and Hichwa, R. PET scan investigations of Huntington’s disease: Cerebral metabolic correlates of neurological features and functional decline. Annals of Neurology, 20:296-303, 1986.
Appendix.
Neurological
1. Tandem
Walk
Evaluation
Instructions: Subject to walk, in a straight
Scale
line, 12 feet, heel to toe.
Assessment: 0 = no missteps after subject has completed first full step; missteps after completion of first full step; 2 = 3 or more missteps, grabbing,
2. Romberg
1 = one or two or falling.
Test
Instructions: Subject to stand with his/her feet together, eyes closed, his/her arms held parallel to the floor, and fingers spread apart. The subject is to maintain this position for 1 min. Assessment: 0 = relatively stable, minimal swaying; maintain balance or falls.
3. Adventitious
I= marked swaying; 2 = subject steps to
Overflow
Instructions: Same as Romberg
Test.
Assessment: 0 = absence of movement of fingers, hands, or arms; 1 = irregular fluttering movement of fingers only; 2 = irregular fluttering movement extended to hands and/ or arms.
4. Tremor Instructions: Same as Romberg Assessment: 0 = no tremor;
Test.
1 = mild, fine tremor;
2 = marked,
fine or coarse tremor.
6. Cerebral Dominance a. Handedness Instructions: Ask subject to demonstrate how he/ she would write, throw a ball, use a tennis racket, strike a match, use scissors, thread a needle, use a broom, use a shovel, deal cards, use a hammer, brush teeth, and unscrew the lid of a jar. Assessment: R-Subject writes with right hand and performs at least seven other activities with right hand; M-Subject writes with right/left hand but performs less than seven other activities with right/left hand; L-Subject writes with left hand and performs at least seven other activities with left hand.
346 b. Footedness Instructions:
Ask subject to demonstrate
Assessment:
R-Subject
how he/she
would kick a ball.
kicks ball with right foot; L-Subject
kicks ball with left foot.
c. Eyedness instructions: Ask subject, with both eyes open, to look at a distant object through a hole in the center of a 3-inch x 5-inch index card that is held with both hands 18 inches in front of the subject. The subject is to close one eye at a time and tell the examiner with which eye closed did he/she lose sight of the object. Assessment: R-Subject loses sight of object with right eye closed; L-Subject of object with left eye closed.
7. Audio-Visual
loses sight
Integration
Instructions: The subject is asked to match a set of tapping sounds with one of three sets of dots presented on a 5-inch x 7-inch index card. The subject is instructed to close his/ her eyes during the tapping. Three practice trials are performed first to ensure that the subject understands the directions. Assessment:
0
q
no error;
1
one error; 2 = two or more errors.
q
8. Stereognosis Instructions: Subject, with eyes closed, is asked to identify an object placed in his/ her hand. Subject is instructed to feel the object with one hand and to take as much time as needed. If subject cannot name the object, he/she is asked to describe for what purpose the object is used. The subject starts with the dominant hand, based on the prior evaluation of handedness, or the hand with which he/she writes, if there is mixed hand dominance. The instructions are repeated at the beginning of the second trial. Assessment:
0
q
no errors;
1 = one error; 2 = more than one error.
9. Graphesthesia Instructions: Subject, with eyes closed, is asked to identify the number written on the tip of his/her forefinger. The order of hands is determined as with stereognosis. Assessment:
10.
Fist-Ring
0 = no errors;
1
q
one error;
2
q
more than one error.
Test
Instructions: The subject is asked to alternate placing his/her hand on the table, in the position of a fist, with the thumb placed either over the knuckles or over the middle phalanges and placing his/ her hand, on the table, in the position of a ring, with the tips of the thumb and forefinger touching and the remaining three fingers extended. The subject is to bring his/ her arm into the upright position between each change in hand position. If the subject does not perform the movement accurately or in a manner that can be appropriately assessed, he/ she is to be stopped, to be reinstructed, and to start the test again. The subject is to repeat each set of hand position changes 15 times.
347
Assessment: 0 = no major disruption of motion after first repetition; errors limited to incomplete extension of fingers in ring position and no more than two hesitancies in the transition from fist to ring or vice versa and no more than one fist/ ring confusion; 1q no major disruption of motion after first repetition or complete breakdown of motion; more than two hesitancies in the transition from fist to ring, difficulty in developing and maintaining a smooth, steady flow of movement, three to four fist/ring confusions, or any total of three but not more than four errors. 2 = major disruption of movement or complete breakdown of motion, or more than four fist Jring hesitations or confusions.
11. Fist-Edge-Palm
Test
Instructions: Ask the subject, using a smooth and steady rhythmic pattern, to touch the table with the side of his/ her fist, the edge of his/ her hand, and the palm of his/ her hand. The subject is to break contact with the surface of the table between each change in hand position, but not to bring the arm back in full flexion. The subject is to repeat this sequence of position changes 15 times. Assessment: 0 q no major disruption of motion afterfirst repetition; errors limited to no more than two hesitancies in the transition from one position to the next and no more than one mistake in hand position. 1 = no major disruption of motion after first repetition or complete breakdown of motion; more than two hesitancies in the transition from one position to another, difficulty in developing and maintaining a smooth, steady flow of movement, three to four position confusions, or any total of three or four errors. 2 = major disruption of movement or complete breakdown of motion, or more than four hesitations or position confusions. 12.
Ozeretski
Test
Instructions: The subject is to place both hands on the table, one hand palm down and the other hand in the shape of a fist. The subject is then asked simultaneously to alternate the position of his/her hands in a smooth and steady motion. The subject is asked to repeat this motion 15 times. Assessment: 0 q no major disruption of motion afterfirst repetition; errors limited to no more than two hesitancies in the transition from one position to the next and no more than one mistake in hand position. 1 = no major disruption of motion after first repetition or complete breakdown of motion; more than two hesitancies in the transition from one position to another, difficulty in developing and maintaining a smooth, steady flow of movement, three to four position confusions, or any total of three, but no more than four errors. 2 = major disruption of movement or complete breakdown of motion, or more than four hesitations or position confusions.
13. Memory Instructions: Subject is told four words and is asked to repeat them immediately after they are all presented. If the subject is unable to repeat the four words correctly, they are represented. If the subject still cannot repeat the four words after a total of three presentations of the words, the test is terminated and the subject is given a score of 2 for both parts of the item. If the subject is able to repeat the four words after the initial or two subsequent presentations, he/she is then asked to remember the words as well as possible and told that he/ she will be asked to repeat the words twice later on during the interview. The subject is then asked to recall the four words at 5 and 10 min. Assessment: 0 = Subject remembers all words; Subject remembers fewer than three words.
1 = Subject
remembers
three words; 2
q
348
14. Rhythm Tapping Test Part A instructions: Ask the subject to reproduce exactly the series of taps heard while the subject has eyes closed. The subject may have eyes open while reproducing series of taps. Assessment: 0 = no errors; I = one error of either nondiscrimination between soft and hard sounds, rhythm, or error in number of taps; 2 = more than one error.
Part B Instructions: Ask the subject Assessment: 0 = no errors;
to produce
a series of taps as instructed.
1 = one error; 2 = more than one error.
15. Rapid Alternating Movements Instructions: Ask the subject to place his/ her hands palm down on legs. The subject is to start with his/ her dominant hand and is to slap his/ her leg distinctly with the palm and the back of his/ her hand in an alternating motion. The determination of dominance is as described above (see item 8). The subject is to perform the task 20 times, with both hands, one hand at a time. Assessment: 0 q no major disruption of motion, hesitation, or mistake in hand placement; I of motion or one to two hesitations or mistakes in hand placement; 2 = major disruption of motion or three or more hesitations or mistakes in hand placement.
= no major disruption
16. Finger-Thumb Opposition Instructions: Ask the subject to place both hands palm up with fingers fully extended on his/ her legs. The subject is to start with his/ her dominant hand and is to touch the tip of his/ her fingers with the tip of his/her thumb, from forefinger to pinky, returning to forefinger, for a total of IO repetitions. Assessment: 0 = no major disruption of motion and no more than one mistake; I = no major disruption of motion or two to three mistakes; 2 = major disruption of motion or four or more mistakes.
17. Mirror Movements Instructions: The subject’s hand, which is not performing the Finger-Thumb Test, is observed for parallel movements of the fingers and thumb. Assessment: 0 = no observable repetitive movements of the fingers;
Opposition
movements of the fingers; I = minor, inconsistent, 2 = consistent, distinctive movements of the fingers.
or
18. Extinction (Face-Hand Test) Instructions: The subject is seated, with hands resting palm down, on his/her knees and with eyes closed. The subject is told that he/she will be touched on either the cheek, hand, or both, and is to say where he/she has been touched. If the subject names just one touch, he/she is asked-the first time this occurs only-if he/she felt a touch anywhere else. The simultaneous touching is done in the following order: right cheek-left hand, left cheek-right hand, right cheek-right hand, left cheek-left hand, both hands, and both cheeks.
349 Assessment:
0 = no errors;
20. Right/Left
1 = one error; 2 = more than one error.
Confusion
Instructions: Subject is asked to point to his/her right foot, left hand; place his/her right hand to left shoulder, left hand to right ear; point to examiner’s left knee, right elbow; with examiner’s arms crossed, point to examiner’s left hand with his/ her right hand, and with examiner recrossing arms, point to examiner’s right hand with his] her left hand. Assessment:
0
q
no errors;
1 = one error; 2 = two or more errors.
21. Synkinesis Instructions: Subject is instructed to follow the cap of a pen with his/ her eyes only as it is moved between extremes of horizontal gaze. If the subject moves his/ her head, the subject is asked to keep his/ her head still and follow the cap of a pen with the eyes only. Assessment: when specifically still.
0 = no movement of the head; 1 = movement of the head on first trial but not told to keep head still; 2 = movement of the head even when told to keep head
22. Convergence Instructions: Subject is instructed toward the subject’s nose.
to follow the cap of a pen with his/ her eyes as it is moved
Assessment: 0 = both eyes converge on object; 1 = one or both eyes are unable to converge completely, but can converge more than halfway; 2~ one or both eyes fail to converge more than halfway.
23. Gaze lmpersistence Instructions: Subject is instructed to fix his/ her gaze on the cap of a pen at a 45 o angle in the horizontal plane of the right and left visual fields for 30 sec. Assessment: 0 = no deviation from fixation; deviation from fixation before 20 sec.
1 = deviation
from fixation
after 20 set; 2 =
24. Finger to Nose Test Instructions: The subject is instructed tip of his/ her index finger.
to close eyes and touch the tip of his/ her nose with the
Assessment: 0 = no intention tremor or passpointing; pointing; 2 = marked intention tremor or passpointing.
25. Glabellar
1 = mild intention
tremor
or pass-
Reflex
Instructions: Subject is instructed to fix his/ her gaze on a point across the room. The subject is approached from above the forehead outside of the visual field, and the examiner taps the glabellar region 10 times with the index finger. Assessment: 0 = three or fewer blinks; 1 = four or five full blinks, or more than six partial or full blinks; 2 = six or more full blinks.
350 26. Snout
Reflex
Instructions: Subject is instructed subject’s philtrum.
to relax, and the examiner
presses his finger against the
Assessment: 0 = no contraction of the orbicularis orris (or puckering contraction of the orbicularis orris (or puckering of the lips).
of the lips); 2 = any
27. Grasp Reflex Instructions: The subject is instructed not to grab, and the examiner strokes the inside of the subject’s palm between the index finger and thumb. This procedure is repeated a second time with the subject being asked to spell the word “help” backwards. Assessment: 0 = no flexion of the subject’s fingers; 1= mild flexion of the subject’s fingers on first trial or flexion of any kind on second trial; 2 q marked flexion of the subject’s fingers on first trial.
28. Suck Reflex Instructions: The examiner between the subject’s lips. Assessment:
places the knuckle of a flexed index finger or tongue depressor
0 = no movement;
2
q
any pursing
or sucking
motion
by the subject’s lips.