Visuospatial function predicts one-week motor skill retention in cognitively intact older adults

Abstract

Motor learning declines with aging, such that older adults retain less motor skill after practice compared to younger adults. However, it remains unclear if these motor learning declines are related to normal cognitive changes associated with aging. The purpose of this study was to examine which cognitive domains would best predict the amount of retention on a motor task one week after training in cognitively intact older adults. Twenty-one adults ages 65 to 84 years old were assessed with Repeatable Battery for the Assessment of Neuropsychological Status, which assesses five cognitive domains (immediate and delayed memory, visuospatial/constructional, language, and attention). Participants also completed one training session of a functional upper extremity task, and were re-tested one week later. Stepwise regression indicated that the visuospatial domain was the only significant predictor of how much skill participants retained over one week, with a visual perception subtest explaining the most variance. Results from this study support previous work reporting that older adults' capacity for motor learning can be probed with visuospatial tests. These tests may capture the structural or functional health of neural networks critical for skill learning within the aging brain, and provide valuable clinical insight about an individual's unique rehabilitation potential.

Introduction

Motor learning declines with aging, such that older adults tend to learn slower and retain less motor skill than younger adults [1,2]. Given the concurrence of aging and cognitive decline [3–7], poorer motor learning may, in part, be linked to normal cognitive changes associated with aging. Studies have shown that memory deficits do not account for motor learning deficits [8–11], suggesting that other cognitive impairments may instead interfere with learning a motor skill. For example, in patients ages 65 to 89 diagnosed with amnestic Mild Cognitive Impairment (MCI), their ability to retain a motor skill may be related to visuospatial impairments rather than their memory impairments [12]. Visuospatial function has been implicated in other types of motor learning, such as motor sequence learning [13,14], but has not been explored extensively in the learning and retention of more complex motor skills in older adults. To further investigate this relationship in the absence of delayed memory impairments, cognitively intact older adults were assessed with the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) [15]. They then completed a single training session of a functional upper extremity motor task, and were re-tested on the motor task one week later. The purpose of this study was to test whether older adults' motor skill retention was related to their visuospatial function, above and beyond other cognitive domains (namely immediate and delayed memory, language, and attention). We hypothesized that better visuospatial scores would be associated with more retention of a complex motor skill from baseline to follow-up one week later.

Materials and methods

Participants

All human research procedures were approved by the university's Institutional Review Board, in accordance with the Helsinki Declaration. Twenty-one cognitively intact adults ages 65 to 84 years old (six males, 15 females) provided informed consent prior to enrollment. Participants were excluded if any cognitive test score fell 1.5 or more standard deviations below normative data, which is a common demarcation point for Mild Cognitive Impairment [16,17]. Participants were also excluded if they had any significant functional limitations, as evidenced by the Katz Inventory of Activity of Daily Living [18]. Exclusion criteria also included any self-reported history of major neurological (e.g., stroke, seizure, traumatic brain injury) or psychiatric (e.g., bipolar disorder, schizophrenia) disorder. To ensure intact sensorimotor function, grip strength (Jamar hand dynamometer, [19]), functional dexterity (Grooved Pegboard, Lafayette Instruments, [20]), and tactile sensation (Semmes-Weinstein monofilaments, [21]) of both hands were collected.

Neuropsychological Battery

All participants completed the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS), which is a widely-used cognitive measure that uses 12 standardized tests to assess the following five cognitive domains as Indexes: Immediate Memory, Visuospatial/Constructional, Language, Attention, and Delayed Memory. A Total Scale score indicating global cognition is also determined by combining all five Index scores. Index and Total scores are age-corrected standard scores (Mean=100, SD=15) based on normative information from the assessment manual; higher values indicate better function. Generally speaking, age-corrected scores represent the participant's cognitive status relative to normative values from age-matched peers, such that the age-corrected score may be interpreted as the participant's cognitive status regardless of age.

Motor skill retention

Motor skill retention was measured using a functional upper extremity motor task. This task was selected for several reasons. First, it is feasible and efficacious for motor skill learning in older adults [22,23] and is retainable [24,25]. Second, it has concurrent and ecological validity with more traditional point-to-point reaching paradigms [26] that have been used previously to quantify retention in more cognitively impaired patients [10] yet is more functional [27].

One trial of the motor task was comprised of five repetitions to three different targets placed radially around a constant start location at a distance of 16 cm; thus, each trial equaled 15 repetitions total. The start location and all three targets were cups that were 9.5 cm in diameter and 5.8 cm in height. Additional details regarding the motor task apparatus, including a schematic, have been published elsewhere (Schaefer and Hengge 2016; Schaefer and Duff 2017). For each repetition, participants used their nondominant hand to acquire and transport two raw kidney beans from the start location to one of the three target locations with a conventional plastic spoon. At the start of each trial, participants' first repetition was out to the ipsilateral target cup, next to the center target cup, and then to the contralateral cup, relative to the hand used. As noted above, participants repeated this sequence five times to complete the trial. Each trial began when the participants picked up the spoon and ended when the last two beans were dropped into the final cup, yielding a ‘trial time’ as the measure of performance. Time continued to elapse in the event of any unsuccessful attempts (e.g., only one bean was placed into a target cup per repetition); thus, any errors that would have occurred during a trial would be accounted for in the performance measure. Performing this task with the nondominant hand is by design to ensure that the task is under-practiced and not over-learned, particularly in older adults [28], such that participants have the potential to show practice effects without confounds of floor or ceiling effects [29]. A modified Edinburgh Handedness Inventory was used to identify participants' nondominant hand [30].

As stated above, the measure of performance was the time taken to complete the 15 repetitions (i.e. “trial time”), with lower times indicating better performance, as participants were instructed to “move as quickly yet as accurately as possible.” All trials were timed to the nearest 100^th of a second via stopwatch. Participants were allowed to adopt any movement pattern during training (i.e., they were not required to move or hold the spoon in any specified manner with their nondominant hand), thereby facilitating exploratory attempts for discovering successful movement strategies for completing the task (see [31]).

After one familiarization trial to ensure participants understood the task, they completed 10 trials. The first trial served as their baseline performance. This small dose of training has also been shown to be sufficient for determining longer-term acquisition and retention [24,32]. Participants were then re-tested a week later on a follow-up trial to identify any measureable skill retention across one week.

Motor skill retention was selected as the primary dependent variable because motor learning is defined as a relatively permanent change in motor performance due to practice or experience [33]. The amount of motor skill retention at one week relative to baseline performance was calculated using Equation 1.

$$\text{retention}(\%)=\left[\left(\text{baseline}–\text{follow}-\text{up}\right)/\text{baseline}\right]\times 100$$ (Eq.1)

Positive values indicated more retention. Normalizing the amount of retention accounts for variations in movement speed or performance on the motor task between participants at baseline [34].

Statistical analysis

The SAS® statistical software program JMP Pro 12 (SAS Institute Inc., Cary, NC) was used for all statistical analysis (α = 0.05). The five individual RBANS Index scores were entered into a backwards elimination stepwise regression analysis as predictors of skill retention. This procedure was the same as in the previous study [12] in order to test the replicability of these findings, in spite of many known limitations of retrospective stepwise regression in general (e.g. [35]). Only Index scores that significantly contributed to the variance in the retention variable were included in the final model based on the criterion-to-remove of p > 0.05. Multiple linear regression was then used to determine which subtests within any significant Indexes were most related to retention. Subtests were entered in a single step into this regression model. Any correlation coefficients (r) greater than 0.59 were considered to be strong, between 0.30 and 0.59 were moderate, and below 0.30 were weak effect sizes (Cohen, 1988).

Results

Group means (and standard deviations) and medians of age, education, grip strength, functional dexterity, and all RBANS Index scores are provided in Table 1. All participants had intact tactile sensation in the tested hand (finest Semmes-Weinstein monofilament detectable, n=20; next finest detectable, n=1). RBANS Total and Index scores had mean and median values ∼100, including that of the Delayed Memory Index, which supports that this sample was largely cognitively intact.

Table 1.

Participant characteristics.

	Mean ± SD	Median	Range
Age (years)	72.9 ± 6.4	74	65-84
Education (years)	15.9 ± 3.2	16	12-24
Grip strength (kg)	22.7 ± 5.5	23.3	12.3-31.6
Grooved Pegboard (s)	101.4 ± 28.5	92.6	71.3-192.7
RBANSa Total Scale Index	105.1 ± 10.8	102	92-136
Immediate Memory Index	103.1 ± 12.0	103	85-129
Visuospatial/Constructional Index	104.4 ± 12.1	105	84-126
Language Index	100.9 ± 11.1	101	82-125
Attention Index	110.5 ± 11.7	115	85-128
Delayed Memory Index	100.1 ± 12.4	101	81-129

N = 21; 6 males and 15 females.

^aRBANS = Repeatable Battery for the Assessment of Neuropsychological Status. Scores are age-corrected, with a normal score of 100 and with a standard deviation of 15.

Performance on the motor task across all trials is shown in Figure 1. Overall, participants improved rapidly from a mean±SD baseline performance of 62.83±12.32 s to 56.71±7.34 s on trial 10, consistent with previous findings [22]. To test the extent to which participants retained these improvements one week later, performance at the one-week follow-up was compared to that at baseline (Eq. 1). On average, retention was 3.22±20.10% (95% CI [-5.93, 12.36]). While statistically this suggests that the group, on average, showed little retention, the large standard deviation indicated a wide range of retention scores. That is, some participants retained little to no skill, while others did. Bivariate analysis indicated that the amount of retention was unrelated to Total Scale Index scores (p=0.11), consistent with previous findings [12]. However, backwards elimination indicated that the Visuospatial/Constructional Index (standardized β=0.56; r=0.56; adjusted r=0.52; p=0.009) was the only significant cognitive predictor of skill retention, such that higher (better) scores were associated with more retention (Fig. 2A). The strength of this effect was considered moderate. All other Index scores for Immediate Memory, Language, Attention, and Delayed Memory were eliminated in the stepwise regression due to lack of significance (all p>0.05).

Fig. 1.

Mean ± standard error task performance for baseline, the nine remaining trials, and one-week follow-up trial. Task performance on the y-axis was measured as the time taken to complete each trial, yielding ‘trial time’ in which lower trial times indicate better task performance.

Fig. 2.

Motor task results were plotted for all participants as a function of the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) Visuospatial/Constructional Index score. Greater values along the x-axis indicate better Index scores. R² and p values are reported for reference. A: Motor skill retention at one week is expressed as a percentage of baseline performance (Eq. 1), with more positive values indicating better retention. B: Baseline performance during the initial testing session is expressed in seconds, with lower times indicating better performance.

Because the motor task itself is visuospatial in nature, requiring visually guided reaching to different spatial locations, it is plausible that participants' baseline performance could also be related to their visuospatial ability. However, baseline performance was not significantly related to Visuospatial/Constructional Index score (p=0.22) (Fig. 2B). This indicates that participants' change in motor skill due to practice/experience, rather than their ability to navigate the task at baseline, is dependent on visuospatial abilities.

Further analysis determined which of the two visuospatial tests that comprise the Visuospatial/Constructional Index explained the most variance in one-week skill retention: Figure Copy and Line Orientation. This was done to explore which aspects of the visuospatial domain may be most predictive of retention among older adults. Multiple linear regression showed that only the Line Orientation subtest was related to skill retention (standardized β=0.52; p=0.02); Figure Copy was not significant (p=0.15). (Assumptions of no multicollinearity were verified; VIF=1.07). For example, a participant with raw score of 20 (age-adjusted z-score=1.29) on Line Orientation improved by over 30% on the motor task from baseline to follow-up, whereas a participant with a raw score of 10 (z-score=-2.28) was ∼42% worse at follow-up compared to baseline, even though both participants had similar Figure Copy scores (17 (z-score=-0.44) and 18 (z-score=-0.059), respectively).

Discussion

This study addressed whether declines in motor skill learning with aging may, in part, be linked to age-related cognitive decline. Consistent with previous findings [12], motor skill retention was related to visuospatial function in cognitively intact older adults. Furthermore, underlying motor learning processes may be more dependent on visual perception (measured with Line Orientation) than visuoconstruction (measured with Figure Copy) [36], although other visuospatial functions not tested by the RBANS may also be important [13,14,37].

Although the motor task in this study requires participants to use vision to guide their movements to different spatial locations, it is important to note that the RBANS Visuospatial/Constructional Index was unrelated to participants' baseline performance on this motor task, consistent with previous studies [12,38]. Because the Visuospatial/Constructional Index correlated with changes in performance (Fig. 2A) rather than to baseline performance (Fig. 2B), it suggests that visuospatial tests may probe the neural processes that are more crucial to learning a movement over time than to the execution of a given movement at a given time. In other studies, visuospatial assessments have been shown to predict rates and amounts of motor skill learning [13,39–41] even in older adults [14,42,43]. For example, surgeons with higher visuospatial ability typically learn complex surgical procedures better and faster than those with lower visuospatial abilities [44–46]. As in our study, visuospatial abilities also tend to not predict baseline surgical performance prior to any training [38], but rather predict the amount of skill learning [47]. One explanation is that visuospatial tests may probe the structural or functional health of critical neural structures or networks for skill learning. Structural neuroimaging has shown that various types of motor learning (e.g., sequencing, force production) is correlated with the integrity of white matter tracts connecting premotor and visual cortex and the cerebellum [48–50] as well as with the functional activation of premotor, prefrontal, and parietal regions [48]. Moreover, these frontal-parietal networks may be lateralized for processing information and/or learning different aspects of a complex motor skill (i.e., reaching, grasping, and object manipulation) [51,52]. Future work is needed to determine how older adults' scores on specific visuospatial tests are related to specific white or gray matter regions of interests that have been implicated in motor learning [53].

The Visuospatial/Constructional Index of the RBANS is comprised of only two visuospatial tests: Line Orientation (for visual perception) and Complex Figure Copy (for visuoconstruction). In reality, however, the visuospatial domain is much broader. Future research is therefore needed to determine which tests of visuospatial function, such as visual perception, visual attention, visuospatial working memory, and/or visuoconstruction, are most predictive of older adults' capacity for learning and retaining a motor skill. Determining older adults' capacity for motor learning has significant rehabilitative implications, given that motor learning (also referred to as procedural or errorless learning [54,55]), has great rehabilitative potential for older adults with dementia [56–59]. This and previous studies suggest, however, that the effectiveness of such approaches may depend on the extent of any concomitant visuospatial impairment in these patients [60], and that visuospatial testing may be a viable way for clinicians to screen for ‘non-responders’ who may not benefit as much from more procedurally-based therapies.

The purpose of this study was to test whether older adults' motor skill retention was related to their visuospatial function, above and beyond other cognitive domains (namely immediate and delayed memory, language, and attention). Stepwise regression indicated that visuospatial function was the only significant predictor of how much skill participants retained over one week, with a visual perception subtest explaining the most variance. These findings suggest these visuospatial tests may capture the structural or functional health of neural networks critical for skill learning within the aging brain, and provide valuable clinical insight about cognitive therapeutic responsiveness.

Highlights.

• Visuospatial function predicts one-week motor skill retention in older adults.

• Extent of delayed memory impairment does not affect retention of motor skill.

• Visuospatial tests could determine responsiveness to procedural-based therapies.