Abstract
OBJECTIVES:
Given the need to detect subclinical changes in brain health that sometimes occur with aging in apparently healthy older adults, we assessed whether bimanual gesture imitation performance, simple to assess clinically, can detect age effects and alterations in cognition, olfaction, and movement.
DESIGN:
Cross-sectional study.
SETTING:
Baltimore Longitudinal Study of Aging.
PARTICIPANTS:
Men and women, aged 22 to 101 years, without cognitive impairment, dementia, stroke, Parkinson disease, resting tremor, abnormal muscle tone, or abnormal coordination (N = 507).
MEASUREMENTS:
Bimanual gesture imitation was measured using a test validated in older adults. We assessed (1) cognition, including verbal memory, executive function, attention, visuospatial ability, visuoperceptual speed, and language; (2) manual dexterity with the Purdue Pegboard Test; (3) olfaction, using the 16-item Sniffin’ Sticks Identification Test; (4) upper extremity motor function, using a computer-based finger tapping test; and (5) lower extremity motor function, including 6-meter usual and rapid gait speeds, 400-meter walk time, Health ABC Physical Performance Battery, and total standing balance time. Cross-sectional associations between bimanual gesture imitation performance and each measure were examined using linear regression after adjustment for age, sex, race, education, and body mass index. Models with mobility measures also adjusted for height.
RESULTS:
Higher gesture imitation performance was associated with younger age. After adjustment, a worse score was associated with worse olfaction, executive function, and visuospatial ability. Gesture imitation score was not associated with other cognitive measures or motor function.
CONCLUSION:
In persons without clinically detectable neurological conditions, poor bimanual gesture imitation is associated with other indicators of brain health, including olfaction and selected cognitive function domains. Bimanual gesture imitation may be useful clinically to detect subtle brain changes in apparently healthy older adults. J Am Geriatr Soc 67:2581–2586, 2019.
Keywords: bimanual gesture imitation, cognition, lifespan, motor function, olfaction
As a higher-order disorder of sensorimotor integration, apraxia is commonly seen in neurological diseases, such as Alzheimer disease (AD) and stroke, and may contribute to dementia diagnosis in early stages.1–6 Among subtypes of apraxia, ideomotor apraxia is believed to reflect an impaired action production system. Due to insufficient conversion to execution of motor programming, individuals with ideomotor apraxia exhibit deficits in the spatial organization, timing, and sequencing of gestural movements.7 Ideomotor apraxia is typically an impairment in intransitive gestures, such as imitation, whereas ideational apraxia is often an impairment in transitive gestures that involve tools or objects.8,9 In ideomotor apraxia, a disturbance in imitation of meaningless gestures may be one of the earliest symptoms in AD.10–12 Contrary to imitation of meaningful or known gestures (such as “OK”), imitation of meaningless gestures is thought to rely entirely on a “direct” neuroprocessing route from visual input to execution of movement, without input from learned gesture representations.13
However, little is known about gesture imitation performance across the lifespan, which may indicate subclinical changes in sensorimotor function sometimes associated with variation in the rate of brain aging. Clinical research and longitudinal studies have shown that changes in sensory and motor systems, such as difficulty in odor identification and slow gait, may precede the onset of mild cognitive impairment and AD by 5 to 15 years and are important predictors of adverse outcomes, including AD and mobility disability.14 Thus, it is of great importance to develop additional simple screening tests that can detect subtle subclinical changes and identify potential markers of persons at risk and in need of preventive interventions. Understanding gesture imitation in aging and its relationships with sensory, cognitive, and motor functions may be clinically relevant due to its ability to reflect sensorimotor integration and early accelerated changes in brain health with aging.
This study examines bimanual gesture imitation performance across the adult lifespan and its relationships with olfaction, cognition, and movement in a sample of clinically neurologically intact, well-characterized, community-dwelling adults. Both neuroimaging evidence in patient populations and conceptual models of cognitive processes suggest that any damage in neural processing from occipital lobes to primary motor and premotor cortices may lead to ideomotor apraxia.15–17 Motor-related and frontal areas may underlie a relationship between gesture imitation and motor function, including mobility and upper extremity motor function. Right frontal areas, including orbitofrontal cortex, play a key role in processing meaningless actions and are also activated during olfactory processing.18,19 Based on current knowledge about the neuroanatomy of ideomotor apraxia, we hypothesize that bimanual gesture imitation performance would be associated with olfactory function, executive function, visuospatial ability, and motor function that involve movement coordination. We hypothesize that brain health beyond aging alone accounts for the variation of bimanual gesture imitation performance.
METHODS
Study Population
A total of 507 participants were drawn from the Baltimore Longitudinal Study of Aging (BLSA), a population-based study with continuous enrollment that began in 1958. According to the criteria for ideomotor apraxia,7,20 we focused on participants without diagnoses or clinical manifestations of cognitive impairment, dementia, stroke, Parkinson disease, resting tremor, abnormal muscle tone, or abnormal coordination.
Neurological Conditions
Diagnoses of cognitive impairment and dementia follow standard BLSA procedures.21 Diagnoses of Parkinson disease and stroke were based on self-reported information. Resting tremor, muscle tone, and coordination were evaluated by clinicians at clinical visits. Specifically, resting tremor of both hands without counting numbers was first assessed by the examiner. If resting tremor without counting was not observed, participants were asked to count backwards by three starting from 100. Resting tremor with counting of both hands was then assessed by the examiner. Muscle tone of both arms was assessed by the examiner and categorized into normal, spastic, lead pipe only, cogwheeling, and lead pipe and cogwheeling conditions. Coordination was assessed using the finger to nose test and was categorized into normal and abnormal conditions.
Bimanual Gesture Imitation
Bimanual gesture imitation was assessed using an Ideomotor Apraxia Test (IAT), previously validated in older persons.22 The IAT is designed to be short and easy to perform and score. The IAT consists of three one-hand symbolic gestures and seven bimanual meaningless gestures without tools or objects being used. Each gesture is scored from 0 to 3: immediate success scores 3; spontaneous correction, 2; correction after supplementary explanation, 1; and failure, 0. Because we were particularly interested in bimanual imitation of meaningless gestures, we collected data on imitation of seven bimanual gestures from the original IAT since April 2016. The maximal score is 21, with seven bimanual gestures.
Cognitive Function
Cognitive function measures included verbal memory, executive function, attention, visuospatial ability, and visuoperceptual speed23: verbal memory by California Verbal Learning Test (CVLT) immediate recall score; attention using the Trail Making Test (TMT) part A; executive function using the difference between time to complete TMT part B and part A; visuospatial ability using a card rotation test; visuoperceptual speed using the Digit Symbol Substitution Test (DSST); and language using letter and category fluency. For language, a domain score was computed based on the sample mean and SD. Manual dexterity was measured using the Purdue Pegboard Test.
Olfaction
Olfactory function was measured using a 16-item Sniffin’ Sticks Identification Test.24 To eliminate a learning effect, two different versions of the olfactory test were alternated during follow-up.
Motor Function
Upper extremity motor function was measured using a computer-based finger tapping test. For simple tapping, participants were instructed to tap their index finger of the dominant or nondominant hand for 10 seconds as quickly as possible, for three separate trials. For complex tapping, participants were instructed to tap the index of finger of two hands alternately for 10 seconds as quickly as possible, also for three separate trials. The average time per tap across the three trials was used for analysis.
Lower extremity motor function measures included usual and rapid gait speeds over 6 meters, Health ABC Physical Performance battery score,25 400-meter walk time, and total standing balance time.21
Statistical Analysis
Bivariate correlations of bimanual gesture imitation score with demographics and each functional measure of interest were examined using Pearson’s correlation analysis for continuous variables or independent t-test for binary variables. Values of olfactory score and time to complete TMT part A were log transformed due to skewed distributions. Because bimanual gesture imitation score was associated with age, correlations with each functional measure of interest were additionally adjusted for age.
The cross-sectional association between gesture imitation score and each functional measure of interest was examined using multivariable linear regression, after adjustment for age, sex, race, body mass index, and years of education. For olfactory score, models were additionally adjusted for the test version. For lower extremity motor function measures, models were additionally adjusted for height.
In bivariate correlational analysis, significance was set at P < .05. In multivariable linear regressions, due to multiple measures within cognitive and motor domains, a false discovery rate (FDR)-adjusted P < .05 was also reported. Analyses were performed using SAS, version 9.4 (SAS Institute, Inc).
RESULTS
Table 1 shows sample characteristics and bivariate correlations with gesture imitation score. Higher gesture imitation score was associated with younger age (P < .05) (Supplementary Figure S1). There were no sex or racial differences in gesture imitation score (all P > .05). The score was not associated with years of education or body mass index (all P > .05). After controlling for age only, higher imitation score was associated with higher olfactory score, higher CVLT immediate recall score, faster time in delta TMT, faster time to complete TMT part A, and higher scores on the card rotation test and DSST (all P < .05). Gesture imitation score was not associated with letter fluency, category fluency, pegboard performance score, finger tapping performance, or lower extremity motor function (all P > .05).
Table 1.
Sample characteristics and correlations with bimanual gesture imitation score (n = 507)
| Demographics | Value, mean ± SD or No. (%) | Range | r(P value) or MD (P value) | Age-adjusted P value |
|---|---|---|---|---|
|
| ||||
| Age, y | 68.3 ± 14.6 | 22 to 101 | −0.2 (<.001) | |
| Women | 225 (55) | 0.2 (.19) | .167 | |
| Black | 127 (31) | −0.2 (.18) | .107 | |
| Education, y | 17.6 ± 2.4 | 8 to 25 | 0.01 (.84) | .669 |
| Body mass index, kg/m2 | 27.3 ± 5.2 | 16.9 to 52.5 | −0.05 (.23) | .147 |
| Gesture imitation score | 19 ± 2 | 6 to 21 | ||
| Olfaction (n = 429) | 11 ± 3 | 3 to 16 | 0.25 (<.001) | <.001 |
| Cognition | ||||
| CVLT immediate recall | 54 ± 12 | 20 to 80 | 0.16 (<.001) | .023 |
| Delta TMT | 46 ± 31 | −13 to 188 | −0.22 (<.001) | <.001 |
| TMT part A, s | 31 ± 13 | 5 to 120 | −0.17 (<.001) | .044 |
| Card rotation | 91 ± 41 | 0 to 216 | 0.17 (<.001) | .021 |
| DSST | 45 ± 13 | 10 to 89 | 0.22 (<.001) | .004 |
| Letter fluency | 15 ± 4 | 3 to 28 | 0.08 (.084) | .303 |
| Category fluency | 16 ± 4 | 7 to 31 | 0.11 (.015) | .470 |
| Pegboard dominant hand performance, average number of pins from two trials | 13 ± 2 | 5 to 18.5 | 0.15 (.001) | .569 |
| Pegboard nondominant hand performance, average number of pins from two trials | 13 ± 2 | 6 to 18 | 0.18 (<.001) | .089 |
| Motor function | ||||
| Simple dominant hand mean tapping time, s/tap | 0.18 ± 0.03 | 0.12 to 0.30 | −0.06 (.176) | .519 |
| Simple nondominant hand mean tapping time, s/tap | 0.19 ± 0.03 | 0.13 to 0.27 | −0.10 (.025) | .803 |
| Complex mean tapping time, s/tap | 0.16 ± 0.06 | 0.07 to 0.67 | −0.12 (.009) | .290 |
| Usual gait speed, m/s | 1.2 ± 0.2 | 0.4 to 1.9 | 0.09 (.043) | .913 |
| Rapid gait speed, m/s | 1.7 ± 0.4 | 0.5 to 3.4 | 0.12 (.006) | .507 |
| 400-m Time, s (n = 480) | 278 ± 63 | 184 to 625 | −0.13 (.003) | .548 |
| Health ABC PPB score | 2.7 ± 0.6 | 0.2 to 3.8 | 0.12 (.007) | .813 |
| Total standing balance time, s | 80 ± 17 | 2 to 90 | 0.09 (.042) | .850 |
Note: P value was based on Pearson’s correlation analysis or independent t-test, as appropriate. Values of olfactory score and time to complete TMT part A were log transformed due to skewed distributions. Olfactory test version was controlled in the analysis.
Abbreviations: CVLT, California Verbal Learning Test; DSST, Digit Symbol Substitution Test; MD, mean difference; PPB, Physical Performance Battery; TMT, Trail Making Test.
Table 2 shows fully adjusted cross-sectional associations between gesture imitation score and olfactory, cognitive, and motor functions. Higher gesture imitation score remained significantly associated with higher olfactory score (FDR-adjusted P = .005), faster time in delta TMT (FDR-adjusted P = .005), higher visuospatial ability (FDR-adjusted P = .033), and higher DSST score (FDR-adjusted P = .041) (Figure 1). Gesture imitation score was not associated with any motor function measure.
Table 2.
Fully adjusted cross-sectional associations of gesture imitation score with olfactory, cognitive, and motor functions
| Outcomes of interest | Standardized β (raw P value) | FDR-adjusted P value | |
|---|---|---|---|
|
| |||
| Olfaction | .157 (<.001) | .005 | |
| Cognition | CVLT immediate recall | .069 (.090) | .143 |
| TMT part A (higher = worse) | −.065 (.095) | .143 | |
| Delta TMT (higher = worse) | −.137 (<.001) | .005 | |
| Card rotation | .106 (.011) | .033 | |
| DSST | .082 (.018) | .041 | |
| Language | .024 (.559) | .629 | |
| Pegboard dominant hand performance, average number of pins from two trials | .012 (.723) | .723 | |
| Pegboard nondominant hand performance, average number of pins from two trials | .055 (.128) | .165 | |
| Motor function | Simple dominant hand tapping time, s/tap (longer = worse) | .023 (.557) | .927 |
| Simple nondominant hand tapping time, s/tap (longer = worse) | −.013 (.729) | .927 | |
| Complex tapping time, s/tap (longer = worse) | −.051 (.228) | .927 | |
| Usual gait speed, m/s | −.014 (.726) | .927 | |
| Rapid gait speed, m/s | .019 (.601) | .927 | |
| 400-m Time, s (longer = worse) | −.021 (.572) | .927 | |
| Health ABC PPB score | −.003 (.937) | .937 | |
| Total standing balance time, s | −.009 (.811) | .927 | |
Note: All models were adjusted for age, sex, race, body mass index, and years of education; for olfactory score, models were additionally adjusted for test version; for lower extremity motor function measures, models were additionally adjusted for height.
Abbreviations: CVLT, California Verbal Learning Test; DSST, Digit Symbol Substitution Test; FDR, false discovery rate; PPB, Physical Performance Battery; TMT, Trail Making Test.
Figure 1.
Significant associations of gesture imitation score with Z scores of olfaction (purple), card rotation performance (blue), delta Trail Making Test (TMT; orange), and Digit Symbol Substitution Test (DSST; green). The sign of delta TMT was flipped to be consistent with directions of other measures. Olfactory Z score was based on log-transformed olfactory score.
DISCUSSION
We demonstrate, for the first time, the significant effect of age across the adult lifespan on intransitive bimanual gesture imitation performance. Independent of age and multiple other factors, in otherwise healthy-appearing adults, poorer gesture imitation performance is associated with poorer olfaction and selected cognitive functions, but not with motor function. Clinically, these findings suggest that simple easily assessed measures of gesture imitation may offer an additional potential behavioral screening test for early deterioration in brain health.
We found an association between age and bimanual gesture imitation performance, which was in line with previous reports on the age differences on imitation of transitive gestures, proximal and distal gestures, and sequences of movements.26–29 Another prior report on ideomotor apraxia did not find an age effect,22 perhaps due to differences in sample characteristics, sample sizes, and ideomotor assessment. The previous study included 26 older adults, aged 70 to 100 years, while our larger study (n = 507) involved an age range between 22 and 101 years. In addition, the prior study incorporated both one-handed meaningful gestures and bimanual meaningless gestures, while our study only focused on bimanual ideomotor assessment of imitating meaningless gestures. Disturbance in imitation of meaningless gestures may be one of the earliest findings in AD.10,12 Perhaps, imitation of meaningless gestures without tools or objects (ie, intransitive) is more sensitive to early changes in sensorimotor function compared to imitation of meaningful gestures. Future studies are needed to verify the age effect on gesture imitation of meaningless and meaningful gestures across the adult lifespan.
Associations with selected cognitive domains suggest that bimanual gesture imitation may indicate early deficits in conversion from movement planning to execution in healthy-appearing adults. These associations are independent of age, indicating that brain health beyond aging alone accounts for the variation of gesture imitation performance. Why does gesture imitation link to selected cognitive domains, including executive function, visuospatial ability, and visuoperceptual speed? One explanation may be shared brain structures. Recent neuroimaging data have suggested that right frontal regions, which are important for executive function, play a key role in processing meaningless gestures.18 Other studies suggest that imitation of meaningful gestures indicates disrupted neural processing in the “direct” route from visual input to movement execution, whereas imitating meaningless gestures involves additional brain areas, such as occipital and inferior parietal lobes important for visual representations and sensory information interpretation and corpus callosum and premotor and primary motor areas important for movement coordination and execution. We cannot rule out that the observed associations with visuospatial ability and executive function may be partially due to the visually mediated component in these cognitive tests. We did not find associations with other cognitive domains, such as attention, language, and memory. The lack of an association with language may be because there are no semantically meaningful items involved in this bimanual gesture imitation test. Future neuroimaging studies could examine the neural substrates underlying ideomotor praxis in healthy-appearing adults.
We also observed a strong association between gesture imitation and olfaction. Although the underlying mechanism is little understood, AD-related brain structural and functional changes might help explain this association. Recent neuroimaging studies of older adults with and without dementia have shown that poorer olfactory function is associated with an AD neuroimaging signature, such as smaller volumes of hippocampus, entorhinal cortex, and middle temporal lobe.30–32 Gesture imitation may serve as a risk screen for future cognitive impairment. Future research is needed to investigate shared mechanisms underlying olfaction and gesture imitation.
We did not observe any associations between gesture imitation and motor function. We propose three possible explanations. First, the lack of associations with motor function measures may be due to the type of intransitive apraxia test in this study. Previous research has shown that the parietal lobe, important for motor function, links to transitive apraxia, which involves tools or objects, whereas our study uses intransitive apraxia test without tools or objects.18 Second, ideomotor apraxia is mainly due to an insufficient conversion from movement planning to execution, while motor impairment can be affected by damage anywhere in the brain from movement planning to execution or in multiple other organ systems, so that motor impairments due to other causes may have obscured associations. Third, it is possible that our tests of motor function were not sufficiently sensitive to reflect early neurological changes clinically. Future studies could assess whether ideomotor praxis is associated with mobility markers that are more sensitive to brain changes, such as gait variability.
This study has several strengths, including a well-characterized, community-dwelling sample with a wide age range, multiple measures of cognitive and motor phenotypes, and clinical assessment of cognitive impairment, dementia, and subtle neurological signs. Limitations include its cross-sectional design, which does not infer causation, as well as the exceptional health of BLSA participants with high levels of education.
CONCLUSION
Bimanual gesture imitation worsens with age. Poor gesture imitation performance may indicate early deficits of olfactory and selected cognition functions in healthy-appearing adults, perhaps reflecting early declines in brain health. Our findings support the potential for this simple, short, and clinically accessible assessment to serve as a behavioral screen for subtle changes in brain health. Future work is needed to evaluate the ability of gesture imitation testing to predict future states, such as dementia or motor decline, as well as to evaluate the value of change in gesture imitation performance over time.
Supplementary Material
Supplementary Figure S1. A scatterplot of bimanual gesture imitation performance as a function of age with a regression line.
ACKNOWLEDGMENTS
Financial Disclosure: This work was supported by the Intramural Research Program of the National Institute on Aging, National Institutes of Health.
Footnotes
Conflict of Interest: N.C. receives honoraria from UCB Pharma and Eisai. S.A.S. is a consultant for Merck and Biophytis.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article.
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Associated Data
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Supplementary Materials
Supplementary Figure S1. A scatterplot of bimanual gesture imitation performance as a function of age with a regression line.