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Normal Aging and Motor Imagery Vividness: Implications for Mental Practice Training in Rehabilitation
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ORIGINAL ARTICLE
Normal Aging and Motor Imagery Vividness: Implications for Mental Practice Training in Rehabilitation Francine Malouin, PhD, Carol L. Richards, PhD, Anne Durand, PhD ABSTRACT. Malouin F, Richards CL, Durand A. Normal aging and motor imagery vividness: implications for mental practice training in rehabilitation. Arch Phys Med Rehabil 2010;91: 1122-7.
Key Words: Aging; Rehabilitation. © 2010 by the American Congress of Rehabilitation Medicine
Objective: To investigate the effects of normal aging on motor imagery vividness and working memory. Design: Descriptive study with 3 groups. Setting: Laboratory of a university-affiliated research rehabilitation center. Participants: A sample of healthy persons (N⫽80) divided into 3 age groups: young (26⫾5.0y), intermediate (53.6⫾5.4y), and elderly (67.6⫾4.6y). Interventions: Not applicable. Main Outcome Measures: The kinesthetic and visual imagery scores of the Kinesthetic and Visual Imagery Questionnaire and scores from 3 domains of working memory (visuospatial, kinesthetic, verbal). Results: Results revealed that visual motor imagery scores were higher than kinesthetic scores (imagery effect: P⫽.001); however, there was also a significant imagery ⫻ group interaction (P⫽.017). Post hoc analyses showed that only the young and intermediate groups had higher visual than kinesthetic motor imagery scores (P⫽.005 and .001, respectively), indicating a loss of visual motor imagery dominance in the elderly group. There was no group effect (P⫽.963) signifying that the level of motor imagery vividness was comparable between age groups. Significant decreases (17.3% and 22.5%, respectively) in visuospatial working memory scores were found in the intermediate (P⫽.011) and elderly (P⫽.001) groups, whereas a significant reduction (P⫽.01) in kinesthetic working memory scores was observed only in the elderly group (26.7%). There was also an age-related significant decline of visuospatial (r⫽ ⫺.50) and kinesthetic (r⫽⫺.34) working memory. Conclusions: The level of motor imagery vividness does not diminish with age, but the quality changes. The dominance of visual motor imagery lessens with aging resulting in motor imagery modality-equivalence. These motor imagery alterations are associated with an age-related decline in visuospatial and kinesthetic working memory.
VER THE PAST DECADE, mental practice through moO tor imagery has proved beneficial as an adjunct therapy for improving motor function after stroke, brain and spinal cord
From the Department of Rehabilitation, Laval University and Center for Interdisciplinary Research in Rehabilitation and Social Integration (Malouin, Richards), the Institut de Réadaptation en Déficience Physique de Québec (Durand), Quebec City, QC, Canada. Supported by Quebec Provincial Rehabilitation Research Network and the Canadian Institutes of Health Research. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Reprint requests to Francine Malouin, PhD, Center for Interdisciplinary Research in Rehabilitation and Social Integration, IRDPQ, 525 Blvd Hamel East, Quebec City, QC, Canada, G1M 2S8, e-mail: [email protected]. Published online May 31, 2010 at www.archives-pmr.org. 0003-9993/10/9107-00891$36.00/0 doi:10.1016/j.apmr.2010.03.007
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injuries, and Parkinson’s disease and for alleviating phantom pain.1,2 Motor imagery is an active process during which the representation of an action is internally reproduced within working memory without any overt output.3 These internal representations of motor actions are centrally organized and like other representations are stored, modified, and may be retrieved through specific cognitive processes.4 Several experimental investigations have shown that physically executed and internally simulated motor actions share similarities at the neural and functional level. For instance, the movement times of mentally simulated tasks such as walking, arm pointing, and writing are similar to their real execution times, indicating that motor representations share similar temporal characteristics and obey the same motor rules as their actual counterparts.5,6 Moreover, imagined and executed actions induce analogous physiologic autonomic responses,4,7 and brain imaging studies have shown that motor imagery activates brain networks that greatly overlap with those activated by real movements.8,9 The neurocognitive similarities between actual and simulated motor actions have been largely documented in young healthy adults. Because the ability to form internal representations of motor actions is necessary for training with mental practice and that its use in rehabilitation involves aging populations, it is important to investigate how motor imagery ability is modulated with normal aging. The few studies10-14 that have examined the effect of normal aging on motor imagery processes suggest a decline in explicit and implicit motor imagery with normal aging. For instance, studies investigating the influence of age on temporal characteristics of real and simulated movements found deterioration in timing accuracy particularly in motor tasks implying either spatiotemporal (speed-accuracy trade-off paradigm) or dynamic (varying gravity-inertial context) constraints.10-13 Likewise, elderly persons were affected in their ability to implicitly simulate movements of the hands, especially those requiring the largest amplitude of displacement and/or with strong biomechanical constraints.14 Aging has selective effects on mental imagery; more specifically, accessing and activating stored visual memories are particularly deteriorated in the elderly.15,16 Earlier studies15,16 have also shown that the generation and manipulation of mental images is more difficult with aging and that these agerelated deficits are likely associated with a decline in working memory.15,16 Little is known, however, about the influence of List of Abbreviations ANOVA KVIQ
analysis of variance Kinesthetic and Visual Imagery Questionnaire
NORMAL AGING AND MOTOR IMAGERY VIVIDNESS, Malouin
age on the ability to generate vivid images of movements. Based on 1 study17 examining the mental representation of movement, it seems that elderly participants are slightly worse than young participants particularly in relation to motor imagery from an internal perspective. In this study, we investigated the influence of normal aging on the vividness of motor imagery18 and working memory (visuospatial, kinesthetic, verbal).19,20 The vividness (eg, clarity of motor images and intensity of the sensations) was examined with the KVIQ18 wherein visual and kinesthetic modalities of motor imagery are assessed from an internal perspective. Because motor imagery involves the generation and maintenance of motor representations in working memory, it was postulated that deficits in motor imagery vividness would be accompanied by a corresponding decline in working memory. METHODS Participants and Design The study included 80 healthy persons who were divided into 3 age groups: a young group with a mean age ⫾ SD of 26⫾5 years (range, 20 –38y), an intermediate group with a mean age ⫾ SD of 53.6⫾5.4 years (range, 41– 60y), and an elderly group greater than 60 years of age with a mean age ⫾ SD of 67.6⫾4.6 years (table 1). This age division was chosen to include middle-aged adults as done recently in the Mulder et al study17 instead of comparing only young and elderly adults as usually done.10-14 The sample was a convenience sample including participants who had taken part in a previous study on the validation of the KVIQ, which explains that the size of each study group is not homogeneous. Participants were initially recruited through postings on a university campus and at a rehabilitation center. All were physically active and in good physical and mental health as determined by a custom-made questionnaire (Health Status Questionnaire) which was administered by an examiner (clinician: physiotherapist or occupational therapist). The participants were university students, workers, and active retirees (eg, volunteering, arts, sports). The Health Status Questionnaire used for screening purposes includes questions relative to medication, past and present med-
Table 1: Subject Characteristics Characteristics
Age (y) Mean ⫾ SD Range Sex Men Women Imagery experience (%) None Motor occasional Motor regular Nonmotor imagery* Education (%) Primary High school College University
Young (n⫽46)
Intermediate (n⫽15)
Elderly (n⫽19)
26.0⫾5.0 (19.9–37.9)
53.6⫾5.4 (40.6–59)
67.6⫾4.6 (60.8–77.6)
23 23
6 9
9 10
52.2 26.1 13.0 8.7
73.3 6.7 13.3 6.7
52.6 26.3 10.5 5.3
0 6.5 39.1 54.3
0 6.7 13.3 80.0
21.1 15.8 10.5 52.6
*Imagery of nonmoving objects (eg, mental images of a series of words on a shopping list).
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ical history, and other conditions (eg, heart, cancer, neurologic, musculoskeletal problems, vision, hearing, and so on). Subjects with conditions affecting sensory inputs (eg, diabetes, burns) who had been immobilized over the last 6 months (eg, fracture, sprain) or who were taking medication affecting the level of attention and alertness were excluded (based on the examiner’s assessment). All subjects gave informed, written consent for their participation in the study, and the protocol was approved by the ethics committee of the rehabilitation institute where the study took place. Experimental Procedures The participants were assessed by 1 of 3 examiners (physiotherapists and occupational therapist) trained in the administration of the KVIQ.18 First, a questionnaire about motor imagery experience (custom made) was answered and then participants were administered the KVIQ and the working memory tests. The KVIQ assesses both visual and kinesthetic motor imagery. The KVIQ includes 20 items (10 movements in each subscale) representing gestures with different body parts. The KVIQ uses a 5-point scale to rate the clarity of the image and the intensity of the sensations; a score of 5 corresponds to the highest level of imagery and a score of 1 to the lowest. The examiner reads the instructions and records the score. The test-retest reliability of the KVIQ has been confirmed in persons with stroke and age-matched healthy persons with intraclass correlation coefficients ranging from .81 to .90.18 Moreover, the internal consistency has Cronbach alpha values that range from .87 to .94, and a factorial analysis confirmed the bifactorial structure of the KVIQ.18 The administration of the KVIQ followed procedures described previously in detail.18,20,21 To promote motor imagery (internal perspective or first-person perspective), subjects were instructed to see or feel themselves moving their limb (from the inside) rather than seeing somebody else (external imagery or third-person perspective). The participants were required to rate their imagery by using the operational definition of each category (eg, 5⫽ image as clear as seeing), and the numbered scale was used only for computation of the data. Three domains of working memory were assessed: visuospatial, verbal, and kinesthetic.19,20 The procedure involved measuring immediate serial recall (or span measurement) for each type of material. This is a standardized procedure22 wherein the examiner presents a series of items and asks the subject to reproduce it immediately in the same order. For each domain, items are taken randomly from a limited pool of items and are presented sequentially. For each type of material, 5 lists of 2 items were first presented. If the subject could reproduce correctly 3 of the 5 lists, the list length was increased by 1 item; otherwise, testing was interrupted. The verbal stimuli were taken from a set of 9 frequent and imaginable monosyllabic words presented in the auditory modality. In the visuospatial condition, the examiner tapped on a series of 9 blocks presented in a random arrangement in front of the subjects. The subject was asked to reproduce the sequence by tapping on the same blocks.23 In the kinesthetic condition, the same standardized procedure was used as described previously, but the stimuli were constructed so as to test working memory for movements. The examiner produced passively a series of gestures, and the subject (blindfold) was asked to reproduce them. The gestures involved unilateral and bilateral lower-limb movements as well as movements involving the trunk and the upper and lower limbs.20 Arch Phys Med Rehabil Vol 91, July 2010
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Data Analyses For each KVIQ subscale, scores for the 10 items were summed, and the total score for each subject (maximum score⫽50 for each subscale) was averaged in each group. For working memory tests, the number of sequences and the number of items correctly recalled were converted into the percent of the maximal possible score, and the percent score for the 2 parameters was averaged.20 To determine the effect of age on motor imagery vividness, the KVIQ scores were compared by using a 2 ⫻ 2 ANOVA with repeated measures for 2 factors, group (young, intermediate, elderly) and imagery modality (visual, kinesthetic), followed by the post hoc Bonferroni procedure (after confirmation of data normality and variance homogeneity). To determine whether working memory ability was affected by age, for each dimension, a between-groups analysis was performed with a 1-way ANOVA (young, intermediate, elderly). The relationship between visual and kinesthetic imagery and between working memory and age was studied with the r Pearson product-moment correlation. The statistical level of significance was set at .05. Statistical tests were performed with SPSSa for Windows. RESULTS Figure 1 shows the mean KVIQ scores for the visual and kinesthetic subscales for the 3 age groups. Results from the ANOVA analysis (imagery and group) revealed that visual imagery scores were higher than kinesthetic imagery scores (imagery effect: F1,78⫽22.07, P⫽.001); however, there was also a significant imagery ⫻ group interaction (F1,78⫽4.27, P⫽.017). Post hoc analyses showed that visual imagery scores were higher than kinesthetic scores in the young (P⫽.005) and intermediate groups (P⫽.001) but not in the elderly group (P⫽.427). Lastly, there was no group effect (F1,78⫽.37, P⫽.963), indicating that the level of imagery was comparable between age groups. Figure 2 shows individual visual scores relative to corresponding kinesthetic scores for each group. Visual scores were generally higher (data points above the line) than kinesthetic scores except in the elderly group. The strength of the relationship between imagery modalities (visual
Fig 2. Relationship between visual and kinesthetic imagery. Scatterplots showing individual visual and kinesthetic imagery scores in each age group. The data points above the diagonal line correspond to participants with larger visual than kinesthetic imagery scores. Note that the data points in the elderly group are clustered along the diagonal line. The diagonal line represents a hypothetic 1 to 1 relationship between the scores from the 2 subscales. Abbreviation: r, Pearson correlation coefficients between visual and kinesthetic scores.
Fig 1. Motor imagery vividness. Mean ⴞ SD visual and kinesthetic imagery scores in the 3 age groups. In contrast to the young and intermediate groups, there was no difference between visual and kinesthetic imagery scores in the elderly group. *Pⴝ.005, †Pⴝ.001. Abbreviation: NS, not statistically significant.
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and kinesthetic) is reflected by the Pearson correlation coefficients. The strongest relationship (r⫽.68, P⬍.01) was found in the elderly group and the lowest (r⫽.01, P⬎.10) in the intermediate group; in the young group, the correlation (r⫽.33, P⬎.10) was in-between.
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Fig 3. Effect of age on working memory. (A) Mean ⴞ SD visuospatial, kinesthetic, and verbal working memory scores for each age group. The young group had larger visuospatial scores compared with the †intermediate (Pⴝ.01) and *elderly group (Pⴝ.001). Significant differences in kinesthetic working memory were found between the young group and *elderly group (Pⴝ.001). There was no significant difference between groups for verbal working memory. (B and C) Scatterplots showing individual working memory scores relative to age for the visuospatial and kinesthetic working memory (B) and verbal working memory (C). Abbreviation: r, Pearson correlation coefficient.
Results from the ANOVA revealed a group effect (fig 3A) for the visuospatial (F2,74⫽11.316, P⫽.001) and kinesthetic working memory (F2,77⫽4.610, P⫽.013). Post hoc analyses indicated that the young group had higher visuospatial memory scores compared with the intermediate group (P⫽.011) and the elderly group (P⫽.001). For the kinesthetic working memory, mean scores in the young group were larger (P⫽.01) than those in the elderly group only. There was no group effect for verbal working memory (F2,77⫽1.375, P⫽.259). Table 2 reports the decrease in working memory relative to the young group in the other 2 groups for the 3 domains of working memory. Although the intermediate and elderly groups showed a substantial decrease in visuospatial working memory (17.3%), the reduction for the kinesthetic domain in the intermediate group was less (6.6%) and 4 times smaller than that in the elderly group, a finding that suggests kinesthetic working memory to be affected by age later than visuospatial. There was a negative correlation between age and working memory scores (fig 3B, C) indicative of a decline with age. This age-related decline was significant for visuospatial (r⫽⫺.50, P⬍.001) and kinesthetic
Table 2: The Percent Decrease in Working Memory Relative to the Young Group for Each Domain of Working Memory in the Other 2 Groups Group/Domains
Intermediate Elderly
Visual (%)
Kinesthetic (%)
Verbal (%)
17.3 (P⫽.001) 22.5 (P⫽.001)
6.6 (NS) 26.7 (P⫽.001)
5.4 (NS) 8.7 (NS)
Abbreviation: NS, not statistically significant.
(r⫽⫺.34, P⬍.01) domains but not for verbal domain (r⫽⫺.17, P⬎.10). DISCUSSION In this study, subtle age-related alterations in the features of motor imagery vividness have been disclosed. Findings from the KVIQ scores indicate that motor imagery vividness does not diminish with age, but its quality changes. Indeed, contrary to the other groups, in the elderly group, the perceived vividness was comparable for both modalities resulting in a strong relationship between visual and kinesthetic imagery scores. These findings indicate that the dominance of visual motor imagery lessens with aging, resulting in motor imagery modality equivalence. In fact, visual imagery scores have been repeatedly reported to be larger than kinesthetic scores in healthy adults,18,21,24-26 and this visual motor imagery dominance is preserved after stroke,18,21 in late blindness,27 and after the immobilization of 1 lower limb,27 indicating that visual motor imagery dominance is a robust trait of motor imagery. Previous investigations15,16,28 have reported alterations in the ability to generate and manipulate mental images with age, and, thus, the present results extend these earlier findings to the internal representation of movements (motor imagery). Because past experience with motor imagery in the elderly group was comparable to that in the young group and that the intermediate group (see table 1) with less motor imagery experience still had visual motor imagery dominance, the motor imagery modality equivalence in the elderly group cannot be attributed to greater exposure to motor imagery. On the other hand, a decline in working memory with increasing age, toArch Phys Med Rehabil Vol 91, July 2010
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gether with the significant decrease in 2 domains of working memory in the elderly group, suggest that alterations in the quality of motor imagery vividness could be linked to working memory deficits. The latter findings concur with those from previous investigations15,16,28 showing the role of working memory in relation with specific age effects for the generation and manipulation of mental images. Our results also showed some differences in the education level between groups, particularly the elderly group, which had a larger proportion of participants with a lower educational level. The educational level is known to influence working memory ability (particularly the verbal domain), but there is no clear indication of how this could affect motor imagery vividness for which previous imagery experience and sensorimotor inputs appear to be important determinants.27 Motor imagery involves cognitive processes to retrieve information (eg, visuospatial and kinesthetic) from long-term memory, to monitor intentions and action plans, and to consciously refrain from the physical execution of the action.10,29 Such demands require a lot of attention and loads working memory already deteriorated in the elderly. Indeed, the frontal and prefrontal cortices that are activated during motor imagery play an important role in working memory.29 Interestingly, during memory-related cognitive tasks, elderly people underrecruit and nonselectively recruit these brain regions, which may explain in part why internal movement representation is altered with increasing age.30,31 Such a lack of specificity in brain activations could thus explain motor imagery modality equivalence. Because a similar motor imagery modality equivalence was recently described in young adults after the amputation of 1 lower limb,27 neural factors other than working memory, such as sensorimotor reorganization,32 may play a role in this phenomenon. Our findings that visuospatial working memory yields greater age differences than verbal or kinesthetic concur with earlier reports.33-35 Study Limitations One can ask about the clinical significance of these subtle motor imagery alterations with increasing age. The first hint at subtle changes in motor imagery vividness came from a study comparing scores from the Vividness of Movement Imagery Questionnaire that assesses the clarity of images (visual modality) from the internal (seeing oneself) and external (seeing someone else) perspective.17 Their findings showed that with aging it became slightly more difficult to imagine oneself than someone else. It is difficult to compare our findings with the KVIQ, which assesses both modalities of motor imagery (clarity of images and the intensity of sensations) from an internal perspective,18 with those comparing visual modality from internal versus external perspective; nevertheless, both studies disclosed a change in the quality of motor imagery with increasing age rather than a deterioration in the general level of motor imagery. Although brain activation patterns during visual and kinesthetic motor imagery greatly overlap, a recent functional magnetic resonance imaging study revealed divergent patterns of activation.36 Indeed, while visual imagery activated predominantly the occipital regions and the superior parietal lobules, kinesthetic imagery yielded more activity in motor-associated structures and the inferior parietal lobule, suggesting that visual and kinesthetic imagery are mediated through separate neural systems.36 Thus, although the changes in scores are not significant, the pattern of visual motor imagery scores shows a decline that contrasts with the pattern of kinesthetic imagery. Based on present results, it is tempting to speculate that the neural network associated with visual motor imagery is more Arch Phys Med Rehabil Vol 91, July 2010
sensitive to aging than that for kinesthetic motor imagery. Likewise, the apparent stability of kinesthetic scores over the 3 age groups and the slower decline of kinesthetic working memory suggest kinesthetic motor imagery to be less vulnerable to the effect of aging on motor imagery vividness. The latter suggestions remains hypothetical, and future studies investigating more complex motor tasks are needed to further elucidate this aspect of motor imagery. Thus, the present results suggest that overall participants in their 60s and 70s had a level of motor imagery vividness that compares with young adults, suggesting that mental practice through motor imagery can be used in older populations. However, because the items tested with the KVIQ correspond mainly to simple movements, the results cannot be generalized to more complex tasks that would further load working memory. It is possible that more severe age-related deficits in motor imagery vividness would be disclosed for more demanding motor tasks (eg, multiple sequences of movement) as was found for temporal features of simulated movements for motor tasks involving strong spatiotemporal or biomechanical constraints.10-14 Moreover, because this study involves a minority of elderly subjects, results should not be generalized to all aged subjects. The fact that a loss of visual modality dominance in the elderly group coincided with significant deficits in visuospatial and kinesthetic working memory suggests that the cognitive status should be taken into account before introducing mental practice. Lastly, when planning training strategies, one should remember that the generation of visual representations of movement becomes more difficult in older populations and that this difficulty may increase with the complexity of the task.10,11,13 CONCLUSIONS Although visual motor imagery dominance declines with age, motor imagery vividness is globally preserved in older populations. Present findings suggest that visual motor imagery is possibly more sensitive to aging than kinesthetic imagery and that age-related deficits in working memory are likely associated with a change in the quality of motor imagery with increasing age. Acknowledgment: We thank Daniel Tardif for his assistance in the preparation of the figures. References 1. Jackson PL, Lafleur MF, Malouin F, Richards CL, Doyon J. Potential role of mental practice using motor imagery in neurological rehabilitation. Arch Phys Med Rehabil 2001;82:1133-41. 2. Dickstein R, Deutsch JE. Motor imagery in physical therapist practice. Phys Ther 2007;87:942-53. 3. Decety J, Grèzes J. Neural mechanisms subserving the perception of human actions. Trends Cogn Sci 1999;3:172-8. 4. Jeannerod M. Mental imagery in the motor context. Neurophysiologica 1995;33:1419-32. 5. Decety J, Michel F. Comparative analysis of actual and mental movement times in two graphic tasks. Brain Cogn 1989;11:87-97. 6. Decety J, Jeannerod M. Mentally simulated movements in virtual reality: does Fitts’s law hold in motor imagery? Behav Brain Res 1995;72:127-34. 7. Wuyam B, Moosavi SH, Decety J, Adams L, Lansing RW, Guz A. Imagination of dynamic exercise produced ventilatory responses which were more apparent in competitive sportsmen. J Physiol 1995;482:713-24. 8. Decety J. Do imagined and executed actions share the same neural substrate? Brain Res Cogn Brain Res 1996;3:87-93.
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9. Szameitat AJ, Shen S, Sterr A. Motor imagery of complex everyday movements. An fMRI study. Neuroimage 2007;34:702-13. 10. Skoura X, Papaxanthis C, Vinter A, Pozzo T. Mentally represented motor actions in normal aging I. Age effects on the temporal features of overt and covert execution of actions. Behav Brain Res 2005;165:229-39. 11. Personnier P, Paizis C, Ballay Y, Papaxanthis C. Mentally represented motor actions in normal aging II. The influence of the gravito-inertial context on the duration of overt and covert arm movements. Behav Brain Res 2008;186:273-83. 12. Skoura X, Personnier P, Vinter A, Pozzo T, Papaxanthis C. Decline in motor prediction in elderly subjects: right versus left arm differences in mentally simulated motor actions. Cortex 2008; 44:1271-8. 13. Personnier P, Ballay Y, Papaxanthis C. Mentally represented motor actions in normal aging: III. Electromyographic features of imagined arm movements. Behav Brain Res 2009;206:184-91. 14. Saimpont A, Pozzo T, Papaxanthis C. Aging affects the mental rotation of left and right hands. PLoS One 2009;4(8):e6714. 15. Briggs SD, Raz N, Marks W. Age-related deficits in generation and manipulation of mental images: I. The role of sensorimotor speed and working memory. Psychol Aging 1999;14:427-35. 16. Dror IE, Kosslyn SM. Mental imagery and aging. Psychol Aging 1994;9:90-102. 17. Mulder T, Hochstenbach JB, van Heuvelen MJ, den Otter AR. Motor imagery: the relation between age and imagery capacity. Hum Mov Sci 2007;26:203-11. 18. Malouin F, Richards CL, Jackson PL, Lafleur MF, Durand A, Doyon J. The Kinesthetic and Visual Imagery Questionnaire (KVIQ) for assessing motor imagery in persons with physical disabilities: a reliability and construct validity study. J Neurol Phys Ther 2007;31:20-9. 19. Dolman R, Roy EA, Dimeck PT, Hall CR. Age, gesture span, and dissociations among component subsystems of working memory. Brain Cogn 2000;43:164-8. 20. Malouin F, Belleville S, Richards CL, Desrosiers J, Doyon J. Working memory and mental practice outcomes after stroke. Arch Phys Med Rehabil 2004;85:177-83. 21. Malouin F, Richards C, Durand A, Doyon J. Clinical assessment of motor imagery after stroke. Neurorehabil Neural Repair 2008; 22:330-40. 22. Spreen O, Strauss E. A compendium of neuropsychological tests. 2nd ed. New York: Oxford Univ Pr; 1998.
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23. DeRenzi E, Faglioni P, Previdi P. Spatial memory and hemispheric locus of lesion. Cortex 1977;13:424-33. 24. Hall CR, Martin KA. Measuring movement imagery abilities: a revision of the Movement Imagery Questionnaire. J Mental Imag 1997;21:143-54. 25. Hall CR, Pongrac J, Buckolz E. The measurement of imagery ability. Hum Mov Sci 1985;4:107-18. 26. Atienza F, Balaguer I, Garcia-Merita MA. Factor analysis and reliability of the movement imagery questionnaire. Percept Mot Skill 1994;78:1323-8. 27. Malouin F, Richards CL, Durand A, et al. Effects of practice, visual loss, limb amputation, and disuse on motor imagery vividness. Neurorehabil Neural Repair 2009;23:449-63. 28. Raz N, Briggs SD, Marks W, Acker JD. Age-related deficits in generation and manipulation of mental images: II. The role of dorsolateral prefrontal cortex. Psychol Aging 1999;14:436-44. 29. Jeannerod M. Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 2001;14:103-9. 30. Logan JM, Sanders AL, Snyder AZ, Morris JC, Buckner RL. Under-recruitment and unselective recruitment: dissociable neural mechanisms associated with aging. Neuron 2002;33:827-40. 31. Reuter-Lorenz PA. New visions of the aging mind and brain. Trends Cogn Sci 2002;6:394-400. 32. Bennett PJ, Sekhuler AB, McIntosh AR, Della-Magiore V. The effects of aging on visual memory: evidence for functional reorganization of cortical networks. Acta Psychol 2001;107:249-73. 33. Jenkins L, Myerson J, Joerding JA, Hale S. Converging evidence that visuospatial cognition is more age sensitive than verbal cognition. Psychol Aging 2000;15:157-75. 34. Verhaegen P, Cerella J, Semenec SC, Leo ME, Bopp KI, Steitz DW. Cognitive efficiency modes in old age: performance on sequential and coordinative verbal and visuospatial tasks. Psychol Aging 2002;17:558-70. 35. Jordan T. Age differences in visual and kinesthetic short-term memory. Percept Motor Skills 1978;46:667-74. 36. Guillot A, Collet C, Nguyen VA, Malouin F, Richards CL, Doyon J. Brain activity during visual versus kinesthetic imagery: an fMRI study. Hum Brain Mapp 2009;30:2157-72. Supplier a. Version 11.0; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
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ORIGINAL ARTICLE
Normal Aging and Motor Imagery Vividness: Implications for Mental Practice Training in Rehabilitation Francine Malouin, PhD, Carol L. Richards, PhD, Anne Durand, PhD ABSTRACT. Malouin F, Richards CL, Durand A. Normal aging and motor imagery vividness: implications for mental practice training in rehabilitation. Arch Phys Med Rehabil 2010;91: 1122-7.
Key Words: Aging; Rehabilitation. © 2010 by the American Congress of Rehabilitation Medicine
Objective: To investigate the effects of normal aging on motor imagery vividness and working memory. Design: Descriptive study with 3 groups. Setting: Laboratory of a university-affiliated research rehabilitation center. Participants: A sample of healthy persons (N⫽80) divided into 3 age groups: young (26⫾5.0y), intermediate (53.6⫾5.4y), and elderly (67.6⫾4.6y). Interventions: Not applicable. Main Outcome Measures: The kinesthetic and visual imagery scores of the Kinesthetic and Visual Imagery Questionnaire and scores from 3 domains of working memory (visuospatial, kinesthetic, verbal). Results: Results revealed that visual motor imagery scores were higher than kinesthetic scores (imagery effect: P⫽.001); however, there was also a significant imagery ⫻ group interaction (P⫽.017). Post hoc analyses showed that only the young and intermediate groups had higher visual than kinesthetic motor imagery scores (P⫽.005 and .001, respectively), indicating a loss of visual motor imagery dominance in the elderly group. There was no group effect (P⫽.963) signifying that the level of motor imagery vividness was comparable between age groups. Significant decreases (17.3% and 22.5%, respectively) in visuospatial working memory scores were found in the intermediate (P⫽.011) and elderly (P⫽.001) groups, whereas a significant reduction (P⫽.01) in kinesthetic working memory scores was observed only in the elderly group (26.7%). There was also an age-related significant decline of visuospatial (r⫽ ⫺.50) and kinesthetic (r⫽⫺.34) working memory. Conclusions: The level of motor imagery vividness does not diminish with age, but the quality changes. The dominance of visual motor imagery lessens with aging resulting in motor imagery modality-equivalence. These motor imagery alterations are associated with an age-related decline in visuospatial and kinesthetic working memory.
VER THE PAST DECADE, mental practice through moO tor imagery has proved beneficial as an adjunct therapy for improving motor function after stroke, brain and spinal cord
From the Department of Rehabilitation, Laval University and Center for Interdisciplinary Research in Rehabilitation and Social Integration (Malouin, Richards), the Institut de Réadaptation en Déficience Physique de Québec (Durand), Quebec City, QC, Canada. Supported by Quebec Provincial Rehabilitation Research Network and the Canadian Institutes of Health Research. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Reprint requests to Francine Malouin, PhD, Center for Interdisciplinary Research in Rehabilitation and Social Integration, IRDPQ, 525 Blvd Hamel East, Quebec City, QC, Canada, G1M 2S8, e-mail: [email protected]. Published online May 31, 2010 at www.archives-pmr.org. 0003-9993/10/9107-00891$36.00/0 doi:10.1016/j.apmr.2010.03.007
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injuries, and Parkinson’s disease and for alleviating phantom pain.1,2 Motor imagery is an active process during which the representation of an action is internally reproduced within working memory without any overt output.3 These internal representations of motor actions are centrally organized and like other representations are stored, modified, and may be retrieved through specific cognitive processes.4 Several experimental investigations have shown that physically executed and internally simulated motor actions share similarities at the neural and functional level. For instance, the movement times of mentally simulated tasks such as walking, arm pointing, and writing are similar to their real execution times, indicating that motor representations share similar temporal characteristics and obey the same motor rules as their actual counterparts.5,6 Moreover, imagined and executed actions induce analogous physiologic autonomic responses,4,7 and brain imaging studies have shown that motor imagery activates brain networks that greatly overlap with those activated by real movements.8,9 The neurocognitive similarities between actual and simulated motor actions have been largely documented in young healthy adults. Because the ability to form internal representations of motor actions is necessary for training with mental practice and that its use in rehabilitation involves aging populations, it is important to investigate how motor imagery ability is modulated with normal aging. The few studies10-14 that have examined the effect of normal aging on motor imagery processes suggest a decline in explicit and implicit motor imagery with normal aging. For instance, studies investigating the influence of age on temporal characteristics of real and simulated movements found deterioration in timing accuracy particularly in motor tasks implying either spatiotemporal (speed-accuracy trade-off paradigm) or dynamic (varying gravity-inertial context) constraints.10-13 Likewise, elderly persons were affected in their ability to implicitly simulate movements of the hands, especially those requiring the largest amplitude of displacement and/or with strong biomechanical constraints.14 Aging has selective effects on mental imagery; more specifically, accessing and activating stored visual memories are particularly deteriorated in the elderly.15,16 Earlier studies15,16 have also shown that the generation and manipulation of mental images is more difficult with aging and that these agerelated deficits are likely associated with a decline in working memory.15,16 Little is known, however, about the influence of List of Abbreviations ANOVA KVIQ
analysis of variance Kinesthetic and Visual Imagery Questionnaire
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age on the ability to generate vivid images of movements. Based on 1 study17 examining the mental representation of movement, it seems that elderly participants are slightly worse than young participants particularly in relation to motor imagery from an internal perspective. In this study, we investigated the influence of normal aging on the vividness of motor imagery18 and working memory (visuospatial, kinesthetic, verbal).19,20 The vividness (eg, clarity of motor images and intensity of the sensations) was examined with the KVIQ18 wherein visual and kinesthetic modalities of motor imagery are assessed from an internal perspective. Because motor imagery involves the generation and maintenance of motor representations in working memory, it was postulated that deficits in motor imagery vividness would be accompanied by a corresponding decline in working memory. METHODS Participants and Design The study included 80 healthy persons who were divided into 3 age groups: a young group with a mean age ⫾ SD of 26⫾5 years (range, 20 –38y), an intermediate group with a mean age ⫾ SD of 53.6⫾5.4 years (range, 41– 60y), and an elderly group greater than 60 years of age with a mean age ⫾ SD of 67.6⫾4.6 years (table 1). This age division was chosen to include middle-aged adults as done recently in the Mulder et al study17 instead of comparing only young and elderly adults as usually done.10-14 The sample was a convenience sample including participants who had taken part in a previous study on the validation of the KVIQ, which explains that the size of each study group is not homogeneous. Participants were initially recruited through postings on a university campus and at a rehabilitation center. All were physically active and in good physical and mental health as determined by a custom-made questionnaire (Health Status Questionnaire) which was administered by an examiner (clinician: physiotherapist or occupational therapist). The participants were university students, workers, and active retirees (eg, volunteering, arts, sports). The Health Status Questionnaire used for screening purposes includes questions relative to medication, past and present med-
Table 1: Subject Characteristics Characteristics
Age (y) Mean ⫾ SD Range Sex Men Women Imagery experience (%) None Motor occasional Motor regular Nonmotor imagery* Education (%) Primary High school College University
Young (n⫽46)
Intermediate (n⫽15)
Elderly (n⫽19)
26.0⫾5.0 (19.9–37.9)
53.6⫾5.4 (40.6–59)
67.6⫾4.6 (60.8–77.6)
23 23
6 9
9 10
52.2 26.1 13.0 8.7
73.3 6.7 13.3 6.7
52.6 26.3 10.5 5.3
0 6.5 39.1 54.3
0 6.7 13.3 80.0
21.1 15.8 10.5 52.6
*Imagery of nonmoving objects (eg, mental images of a series of words on a shopping list).
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ical history, and other conditions (eg, heart, cancer, neurologic, musculoskeletal problems, vision, hearing, and so on). Subjects with conditions affecting sensory inputs (eg, diabetes, burns) who had been immobilized over the last 6 months (eg, fracture, sprain) or who were taking medication affecting the level of attention and alertness were excluded (based on the examiner’s assessment). All subjects gave informed, written consent for their participation in the study, and the protocol was approved by the ethics committee of the rehabilitation institute where the study took place. Experimental Procedures The participants were assessed by 1 of 3 examiners (physiotherapists and occupational therapist) trained in the administration of the KVIQ.18 First, a questionnaire about motor imagery experience (custom made) was answered and then participants were administered the KVIQ and the working memory tests. The KVIQ assesses both visual and kinesthetic motor imagery. The KVIQ includes 20 items (10 movements in each subscale) representing gestures with different body parts. The KVIQ uses a 5-point scale to rate the clarity of the image and the intensity of the sensations; a score of 5 corresponds to the highest level of imagery and a score of 1 to the lowest. The examiner reads the instructions and records the score. The test-retest reliability of the KVIQ has been confirmed in persons with stroke and age-matched healthy persons with intraclass correlation coefficients ranging from .81 to .90.18 Moreover, the internal consistency has Cronbach alpha values that range from .87 to .94, and a factorial analysis confirmed the bifactorial structure of the KVIQ.18 The administration of the KVIQ followed procedures described previously in detail.18,20,21 To promote motor imagery (internal perspective or first-person perspective), subjects were instructed to see or feel themselves moving their limb (from the inside) rather than seeing somebody else (external imagery or third-person perspective). The participants were required to rate their imagery by using the operational definition of each category (eg, 5⫽ image as clear as seeing), and the numbered scale was used only for computation of the data. Three domains of working memory were assessed: visuospatial, verbal, and kinesthetic.19,20 The procedure involved measuring immediate serial recall (or span measurement) for each type of material. This is a standardized procedure22 wherein the examiner presents a series of items and asks the subject to reproduce it immediately in the same order. For each domain, items are taken randomly from a limited pool of items and are presented sequentially. For each type of material, 5 lists of 2 items were first presented. If the subject could reproduce correctly 3 of the 5 lists, the list length was increased by 1 item; otherwise, testing was interrupted. The verbal stimuli were taken from a set of 9 frequent and imaginable monosyllabic words presented in the auditory modality. In the visuospatial condition, the examiner tapped on a series of 9 blocks presented in a random arrangement in front of the subjects. The subject was asked to reproduce the sequence by tapping on the same blocks.23 In the kinesthetic condition, the same standardized procedure was used as described previously, but the stimuli were constructed so as to test working memory for movements. The examiner produced passively a series of gestures, and the subject (blindfold) was asked to reproduce them. The gestures involved unilateral and bilateral lower-limb movements as well as movements involving the trunk and the upper and lower limbs.20 Arch Phys Med Rehabil Vol 91, July 2010
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Data Analyses For each KVIQ subscale, scores for the 10 items were summed, and the total score for each subject (maximum score⫽50 for each subscale) was averaged in each group. For working memory tests, the number of sequences and the number of items correctly recalled were converted into the percent of the maximal possible score, and the percent score for the 2 parameters was averaged.20 To determine the effect of age on motor imagery vividness, the KVIQ scores were compared by using a 2 ⫻ 2 ANOVA with repeated measures for 2 factors, group (young, intermediate, elderly) and imagery modality (visual, kinesthetic), followed by the post hoc Bonferroni procedure (after confirmation of data normality and variance homogeneity). To determine whether working memory ability was affected by age, for each dimension, a between-groups analysis was performed with a 1-way ANOVA (young, intermediate, elderly). The relationship between visual and kinesthetic imagery and between working memory and age was studied with the r Pearson product-moment correlation. The statistical level of significance was set at .05. Statistical tests were performed with SPSSa for Windows. RESULTS Figure 1 shows the mean KVIQ scores for the visual and kinesthetic subscales for the 3 age groups. Results from the ANOVA analysis (imagery and group) revealed that visual imagery scores were higher than kinesthetic imagery scores (imagery effect: F1,78⫽22.07, P⫽.001); however, there was also a significant imagery ⫻ group interaction (F1,78⫽4.27, P⫽.017). Post hoc analyses showed that visual imagery scores were higher than kinesthetic scores in the young (P⫽.005) and intermediate groups (P⫽.001) but not in the elderly group (P⫽.427). Lastly, there was no group effect (F1,78⫽.37, P⫽.963), indicating that the level of imagery was comparable between age groups. Figure 2 shows individual visual scores relative to corresponding kinesthetic scores for each group. Visual scores were generally higher (data points above the line) than kinesthetic scores except in the elderly group. The strength of the relationship between imagery modalities (visual
Fig 2. Relationship between visual and kinesthetic imagery. Scatterplots showing individual visual and kinesthetic imagery scores in each age group. The data points above the diagonal line correspond to participants with larger visual than kinesthetic imagery scores. Note that the data points in the elderly group are clustered along the diagonal line. The diagonal line represents a hypothetic 1 to 1 relationship between the scores from the 2 subscales. Abbreviation: r, Pearson correlation coefficients between visual and kinesthetic scores.
Fig 1. Motor imagery vividness. Mean ⴞ SD visual and kinesthetic imagery scores in the 3 age groups. In contrast to the young and intermediate groups, there was no difference between visual and kinesthetic imagery scores in the elderly group. *Pⴝ.005, †Pⴝ.001. Abbreviation: NS, not statistically significant.
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and kinesthetic) is reflected by the Pearson correlation coefficients. The strongest relationship (r⫽.68, P⬍.01) was found in the elderly group and the lowest (r⫽.01, P⬎.10) in the intermediate group; in the young group, the correlation (r⫽.33, P⬎.10) was in-between.
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Fig 3. Effect of age on working memory. (A) Mean ⴞ SD visuospatial, kinesthetic, and verbal working memory scores for each age group. The young group had larger visuospatial scores compared with the †intermediate (Pⴝ.01) and *elderly group (Pⴝ.001). Significant differences in kinesthetic working memory were found between the young group and *elderly group (Pⴝ.001). There was no significant difference between groups for verbal working memory. (B and C) Scatterplots showing individual working memory scores relative to age for the visuospatial and kinesthetic working memory (B) and verbal working memory (C). Abbreviation: r, Pearson correlation coefficient.
Results from the ANOVA revealed a group effect (fig 3A) for the visuospatial (F2,74⫽11.316, P⫽.001) and kinesthetic working memory (F2,77⫽4.610, P⫽.013). Post hoc analyses indicated that the young group had higher visuospatial memory scores compared with the intermediate group (P⫽.011) and the elderly group (P⫽.001). For the kinesthetic working memory, mean scores in the young group were larger (P⫽.01) than those in the elderly group only. There was no group effect for verbal working memory (F2,77⫽1.375, P⫽.259). Table 2 reports the decrease in working memory relative to the young group in the other 2 groups for the 3 domains of working memory. Although the intermediate and elderly groups showed a substantial decrease in visuospatial working memory (17.3%), the reduction for the kinesthetic domain in the intermediate group was less (6.6%) and 4 times smaller than that in the elderly group, a finding that suggests kinesthetic working memory to be affected by age later than visuospatial. There was a negative correlation between age and working memory scores (fig 3B, C) indicative of a decline with age. This age-related decline was significant for visuospatial (r⫽⫺.50, P⬍.001) and kinesthetic
Table 2: The Percent Decrease in Working Memory Relative to the Young Group for Each Domain of Working Memory in the Other 2 Groups Group/Domains
Intermediate Elderly
Visual (%)
Kinesthetic (%)
Verbal (%)
17.3 (P⫽.001) 22.5 (P⫽.001)
6.6 (NS) 26.7 (P⫽.001)
5.4 (NS) 8.7 (NS)
Abbreviation: NS, not statistically significant.
(r⫽⫺.34, P⬍.01) domains but not for verbal domain (r⫽⫺.17, P⬎.10). DISCUSSION In this study, subtle age-related alterations in the features of motor imagery vividness have been disclosed. Findings from the KVIQ scores indicate that motor imagery vividness does not diminish with age, but its quality changes. Indeed, contrary to the other groups, in the elderly group, the perceived vividness was comparable for both modalities resulting in a strong relationship between visual and kinesthetic imagery scores. These findings indicate that the dominance of visual motor imagery lessens with aging, resulting in motor imagery modality equivalence. In fact, visual imagery scores have been repeatedly reported to be larger than kinesthetic scores in healthy adults,18,21,24-26 and this visual motor imagery dominance is preserved after stroke,18,21 in late blindness,27 and after the immobilization of 1 lower limb,27 indicating that visual motor imagery dominance is a robust trait of motor imagery. Previous investigations15,16,28 have reported alterations in the ability to generate and manipulate mental images with age, and, thus, the present results extend these earlier findings to the internal representation of movements (motor imagery). Because past experience with motor imagery in the elderly group was comparable to that in the young group and that the intermediate group (see table 1) with less motor imagery experience still had visual motor imagery dominance, the motor imagery modality equivalence in the elderly group cannot be attributed to greater exposure to motor imagery. On the other hand, a decline in working memory with increasing age, toArch Phys Med Rehabil Vol 91, July 2010
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gether with the significant decrease in 2 domains of working memory in the elderly group, suggest that alterations in the quality of motor imagery vividness could be linked to working memory deficits. The latter findings concur with those from previous investigations15,16,28 showing the role of working memory in relation with specific age effects for the generation and manipulation of mental images. Our results also showed some differences in the education level between groups, particularly the elderly group, which had a larger proportion of participants with a lower educational level. The educational level is known to influence working memory ability (particularly the verbal domain), but there is no clear indication of how this could affect motor imagery vividness for which previous imagery experience and sensorimotor inputs appear to be important determinants.27 Motor imagery involves cognitive processes to retrieve information (eg, visuospatial and kinesthetic) from long-term memory, to monitor intentions and action plans, and to consciously refrain from the physical execution of the action.10,29 Such demands require a lot of attention and loads working memory already deteriorated in the elderly. Indeed, the frontal and prefrontal cortices that are activated during motor imagery play an important role in working memory.29 Interestingly, during memory-related cognitive tasks, elderly people underrecruit and nonselectively recruit these brain regions, which may explain in part why internal movement representation is altered with increasing age.30,31 Such a lack of specificity in brain activations could thus explain motor imagery modality equivalence. Because a similar motor imagery modality equivalence was recently described in young adults after the amputation of 1 lower limb,27 neural factors other than working memory, such as sensorimotor reorganization,32 may play a role in this phenomenon. Our findings that visuospatial working memory yields greater age differences than verbal or kinesthetic concur with earlier reports.33-35 Study Limitations One can ask about the clinical significance of these subtle motor imagery alterations with increasing age. The first hint at subtle changes in motor imagery vividness came from a study comparing scores from the Vividness of Movement Imagery Questionnaire that assesses the clarity of images (visual modality) from the internal (seeing oneself) and external (seeing someone else) perspective.17 Their findings showed that with aging it became slightly more difficult to imagine oneself than someone else. It is difficult to compare our findings with the KVIQ, which assesses both modalities of motor imagery (clarity of images and the intensity of sensations) from an internal perspective,18 with those comparing visual modality from internal versus external perspective; nevertheless, both studies disclosed a change in the quality of motor imagery with increasing age rather than a deterioration in the general level of motor imagery. Although brain activation patterns during visual and kinesthetic motor imagery greatly overlap, a recent functional magnetic resonance imaging study revealed divergent patterns of activation.36 Indeed, while visual imagery activated predominantly the occipital regions and the superior parietal lobules, kinesthetic imagery yielded more activity in motor-associated structures and the inferior parietal lobule, suggesting that visual and kinesthetic imagery are mediated through separate neural systems.36 Thus, although the changes in scores are not significant, the pattern of visual motor imagery scores shows a decline that contrasts with the pattern of kinesthetic imagery. Based on present results, it is tempting to speculate that the neural network associated with visual motor imagery is more Arch Phys Med Rehabil Vol 91, July 2010
sensitive to aging than that for kinesthetic motor imagery. Likewise, the apparent stability of kinesthetic scores over the 3 age groups and the slower decline of kinesthetic working memory suggest kinesthetic motor imagery to be less vulnerable to the effect of aging on motor imagery vividness. The latter suggestions remains hypothetical, and future studies investigating more complex motor tasks are needed to further elucidate this aspect of motor imagery. Thus, the present results suggest that overall participants in their 60s and 70s had a level of motor imagery vividness that compares with young adults, suggesting that mental practice through motor imagery can be used in older populations. However, because the items tested with the KVIQ correspond mainly to simple movements, the results cannot be generalized to more complex tasks that would further load working memory. It is possible that more severe age-related deficits in motor imagery vividness would be disclosed for more demanding motor tasks (eg, multiple sequences of movement) as was found for temporal features of simulated movements for motor tasks involving strong spatiotemporal or biomechanical constraints.10-14 Moreover, because this study involves a minority of elderly subjects, results should not be generalized to all aged subjects. The fact that a loss of visual modality dominance in the elderly group coincided with significant deficits in visuospatial and kinesthetic working memory suggests that the cognitive status should be taken into account before introducing mental practice. Lastly, when planning training strategies, one should remember that the generation of visual representations of movement becomes more difficult in older populations and that this difficulty may increase with the complexity of the task.10,11,13 CONCLUSIONS Although visual motor imagery dominance declines with age, motor imagery vividness is globally preserved in older populations. Present findings suggest that visual motor imagery is possibly more sensitive to aging than kinesthetic imagery and that age-related deficits in working memory are likely associated with a change in the quality of motor imagery with increasing age. Acknowledgment: We thank Daniel Tardif for his assistance in the preparation of the figures. References 1. Jackson PL, Lafleur MF, Malouin F, Richards CL, Doyon J. Potential role of mental practice using motor imagery in neurological rehabilitation. Arch Phys Med Rehabil 2001;82:1133-41. 2. Dickstein R, Deutsch JE. Motor imagery in physical therapist practice. Phys Ther 2007;87:942-53. 3. Decety J, Grèzes J. Neural mechanisms subserving the perception of human actions. Trends Cogn Sci 1999;3:172-8. 4. Jeannerod M. Mental imagery in the motor context. Neurophysiologica 1995;33:1419-32. 5. Decety J, Michel F. Comparative analysis of actual and mental movement times in two graphic tasks. Brain Cogn 1989;11:87-97. 6. Decety J, Jeannerod M. Mentally simulated movements in virtual reality: does Fitts’s law hold in motor imagery? Behav Brain Res 1995;72:127-34. 7. Wuyam B, Moosavi SH, Decety J, Adams L, Lansing RW, Guz A. Imagination of dynamic exercise produced ventilatory responses which were more apparent in competitive sportsmen. J Physiol 1995;482:713-24. 8. Decety J. Do imagined and executed actions share the same neural substrate? Brain Res Cogn Brain Res 1996;3:87-93.
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23. DeRenzi E, Faglioni P, Previdi P. Spatial memory and hemispheric locus of lesion. Cortex 1977;13:424-33. 24. Hall CR, Martin KA. Measuring movement imagery abilities: a revision of the Movement Imagery Questionnaire. J Mental Imag 1997;21:143-54. 25. Hall CR, Pongrac J, Buckolz E. The measurement of imagery ability. Hum Mov Sci 1985;4:107-18. 26. Atienza F, Balaguer I, Garcia-Merita MA. Factor analysis and reliability of the movement imagery questionnaire. Percept Mot Skill 1994;78:1323-8. 27. Malouin F, Richards CL, Durand A, et al. Effects of practice, visual loss, limb amputation, and disuse on motor imagery vividness. Neurorehabil Neural Repair 2009;23:449-63. 28. Raz N, Briggs SD, Marks W, Acker JD. Age-related deficits in generation and manipulation of mental images: II. The role of dorsolateral prefrontal cortex. Psychol Aging 1999;14:436-44. 29. Jeannerod M. Neural simulation of action: a unifying mechanism for motor cognition. Neuroimage 2001;14:103-9. 30. Logan JM, Sanders AL, Snyder AZ, Morris JC, Buckner RL. Under-recruitment and unselective recruitment: dissociable neural mechanisms associated with aging. Neuron 2002;33:827-40. 31. Reuter-Lorenz PA. New visions of the aging mind and brain. Trends Cogn Sci 2002;6:394-400. 32. Bennett PJ, Sekhuler AB, McIntosh AR, Della-Magiore V. The effects of aging on visual memory: evidence for functional reorganization of cortical networks. Acta Psychol 2001;107:249-73. 33. Jenkins L, Myerson J, Joerding JA, Hale S. Converging evidence that visuospatial cognition is more age sensitive than verbal cognition. Psychol Aging 2000;15:157-75. 34. Verhaegen P, Cerella J, Semenec SC, Leo ME, Bopp KI, Steitz DW. Cognitive efficiency modes in old age: performance on sequential and coordinative verbal and visuospatial tasks. Psychol Aging 2002;17:558-70. 35. Jordan T. Age differences in visual and kinesthetic short-term memory. Percept Motor Skills 1978;46:667-74. 36. Guillot A, Collet C, Nguyen VA, Malouin F, Richards CL, Doyon J. Brain activity during visual versus kinesthetic imagery: an fMRI study. Hum Brain Mapp 2009;30:2157-72. Supplier a. Version 11.0; SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.
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